Resistance of the house fly Musca domestica (Diptera: Muscidae)to lambda-cyhalothrin: mode of inheritance, realized heritability,and cross-resistance to other insecticides

Naeem Abbas • Hafiz Azhar Ali Khan •

Sarfraz Ali Shad

Accepted: 20 February 2014

� Springer Science+Business Media New York 2014

Abstract Lambda-cyhalothrin, a pyrethroid insecticide,

has been used frequently for the control of house flies,

Musca domestica L., worldwide including Pakistan. To

assess the resistance risk and design a resistance manage-

ment strategy, a house fly population was exposed to

lambda-cyhalothrin in the laboratory to assess inheritance

and heritability, and cross-resistance to other insecticides,

including different chemical classes. After 11 generations

of selection, the population developed 113.57-fold resis-

tance to lambda-cyhalothrin compared to the susceptible

population. There was no cross-resistance to bifenthrin and

methomyl, but very low cross-resistance to abamectin and

indoxacarb in the lambda-cyhalothrin selected population

compared to the field population. Synergism bioassay with

piperonyl butoxide and S,S,S-tributylphosphorotrithioate

indicated that lambda-cyhalothrin resistance was associ-

ated with microsomal oxidases and esterases. The LC50

values of F1 (Lambda-SEL $ 9 Susceptible #) and F01(Lambda-SEL # 9 Susceptible $) populations were not

significantly different and dominance (DLC) values were

0.68 and 0.62. The resistance to lambda-cyhalothrin was

completely recessive (DML = 0.00) at highest dose and

completely dominant at lowest dose (DML = 0.95). The

monogenic model of inheritance showed that lambda-cy-

halothrin resistance was controlled by multiple factors. The

heritability values were 0.20, 0.04, 0.003, 0.07 and 0.08 for

lambda-cyhalothrin, bifenthrin, methomyl, indoxacarb and

abamectin resistance, respectively. It was concluded that

lambda-cyhalothrin resistance in house flies was autoso-

mally inherited, incompletely dominant and controlled by

multiple factors. These findings would be helpful to

improve the management of house flies.

Keywords Polygenic resistance � Dominance � Genetics �Realized heritability � Pyrethroid

Introduction

The house fly, Musca domestica L., (Diptera: Muscidae) is

a key pest of poultries and human beings (Axtell 1985). It

is a mechanical vector of more than 100 animal intestinal

diseases such as protozoan (amoebic dysentery), bacterial

(salmonellosis, shigellosis, cholera), helminthic (hook-

worm, roundworms, tapeworms) and viral infections

(Forster et al. 2007; Acevedo et al. 2009). The large

amount of poultry manure which is exposed to high

humidity and temperature can provide ideal conditions for

house fly growth in poultry farms. High-density popula-

tions irritate and stress the poultry workers, hens and

influence the economic of poultry products (Acevedo et al.

2009).

Pyrethroids (e.g. lambda-cyhalothrin), are sodium

channel modulators (Nauen et al. 2012). For a number of

decades, pyrethroids have been extensively used for the

management of various insect pests (especially Diptera;

Electronic supplementary material The online version of thisarticle (doi:10.1007/s10646-014-1217-7) contains supplementarymaterial, which is available to authorized users.

N. Abbas (&) � S. A. Shad (&)

Department of Entomology, Faculty of Agricultural Sciences

and Technology, Bahauddin Zakariya University, Multan,

Pakistan

e-mail: naeemsurbana@gmail.com

S. A. Shad

e-mail: sarfrazshad@bzu.edu.pk

H. A. A. Khan

Institute of Agricultural Sciences, University of the Punjab,

Lahore, Pakistan

123

Ecotoxicology

DOI 10.1007/s10646-014-1217-7

Zhang et al. 2008), due to their effectiveness, environ-

mental safety (or inocuousness), and low toxicity to

mammals (Narahashi et al. 2007). However, extensive and

injudicious use of these insecticides has led to the devel-

opment of resistance in the house fly (Khan et al. 2013a).

Resistance to pyrethroids is reported in many insect pests

such as Bemisia tabaci (Abou-Yousef et al. 2010), S. litura

(F.) (Ahmad et al. 2007) and Helicoverpa armigera (H.)

(Achaleke and Brevault 2010). Resistance to pyrethroids

has also been reported in house fly worldwide, for example,

very high level of resistance to permethrin in Japan

([18,400-fold; Shono et al. 2002) and to beta-cypermethrin

in China (4,420-fold; Zhang et al. 2008).

Major mechanisms involved in pyrethroid resistance are

metabolic detoxification, decreased target site sensitivity

and decreased cuticular penetration (Devonshire 1973; Scott

and Georghiou 1986; Scott 2001). Metabolic resistance to

pyrethroids in insects can be associated with increases in

cytochrome P450 activity, increases in general esterases and

elevated glutathione S-transferases due to gene copy num-

ber, enabling them to overproduce this type of enzyme (Scott

1999; Bass and Linda 2011; Aizoun et al. 2013). Mutations

in the voltage-gated sodium channel gene also contribute to

knockdown resistance (kdr) to pyrethroids (Soderlund and

Knipple 2003). Tian et al. (2011) found that P450-mediated

detoxification and sodium channel-mediated target site

insensitivity are major mechanisms related to pyrethroid

resistance development in house flies.

According to the resistance monitoring reports against

various pyrethroid insecticides in house flies collected from

poultry farms from five regions in Punjab, Pakistan, sig-

nificant levels of resistance have been observed in different

populations (Abbas, Unpublished). Recently, resistance to

different pyrethroids in six house fly strains from dairy

farms has also been reported from Punjab, Pakistan (Khan

et al. 2013a). The poultry farms differ from dairy farms

because these are closed and would be expected to limit the

migration of house flies (Scott et al. 2000). Among the

molecules monitored, lambda-cyhalothrin is currently the

most extensively used on house flies (Khan et al. 2013b).

Analysis of type of inheritance and measurement of

insecticide resistance in pests can give valuable informa-

tion to develop better strategy for the management of

resistance (Ahmad et al. 2007; Zhang et al. 2008). The

genetics of resistance to pyrethroid insecticides has been

studied in many insect pests. For example, cypermethrin

resistance was incompletely recessive, autosomal and

controlled by a single allele in horn fly, Haematobia irri-

tans (L.) (Roush et al. 1986). Similarly, in tobacco bud-

worm, Heliothis virescens (F.), permethrin resistance was

incompletely recessive, autosomal and controlled by one

major gene (Gregory et al. 1988). In diamondback moth,

P. xylostella (L.), and armyworm, S. litura, deltamethrin

resistance was inherited as autosomal, incompletely dom-

inant trait and controlled by multiple genes (Sayyed et al.

2005; Ahmad et al. 2007). In house flies, resistance to

permethrin was found autosomal and incompletely reces-

sive (Shono et al. 2002). Beta-cypermethrin resistance was

controlled by a single gene, autosomally inherited and

incompletely recessive in house flies (Zhang et al. 2008).

However, to our knowledge, the inheritance of resistance to

lambda-cyhalothrin has not been investigated in house fly.

To develop a better resistance management strategy, the

cross-resistance to different insecticides, mode of inheri-

tance and realized heritability of resistance of a lambda-

cyhalothrin selected house fly population was evaluated in

the present study. The aim of the synergism experiment

was to evaluate the mechanism of lambda-cyhalothrin

resistance in house flies.

Materials and methods

Insects

Adult house flies were collected by sweep-netting from a

poultry farm located in Multan (30. 066141N; 71. 68695E),

Punjab, Pakistan. The selected poultry farm used pesticides

heavily for the management of different poultry pests

including house flies (Personal communication; Dr. Arshad

Mehmood, poultry farm owner). About 300 flies were

collected and brought to the laboratory for rearing. The

adults were kept in meshed plastic jars (34 9 17 cm) and

fed on powdered milk mixed with sugar 1:1 ratio by weight

(gram), and cotton wick soaked with water was provided in

separate Petri dish. The larvae were reared on a medium of

powdered milk, sugar, yeast, grass meal and wheat bran at

a ratio of 1.5:1.5:5:5:20 by weight (gram) respectively and

made a paste with 65 ml water (Khan et al. 2013a, c). All

the insects were maintained at 25–27 �C, 60–70 % RH and

14:10 light: dark photoperiod. The susceptible population

was collected from an area with no insecticide use and

maintained in the laboratory without insecticides.

Insecticides and synergists

Commercial-grade formulated insecticides used for bioas-

says included pyrethroids: lambda-cyhalothrin (Karate

2.5EC, Syngenta), bifenthrin (Talstar 10EC, FMC), and

non pyrethroids; methomyl (Lannate 40SP; DuPont), ind-

oxacarb (Steward 15SC, DuPont), abamectin (Alarm

1.8EC, DJC), Piperonyl butoxide (PBO; Sigma Ltd, UK),

an inhibitor of cytochrome P450 monooxygenases

(microsomal oxidases) and of esterases, and S,S,S-tribu-

tylphosphorotrithioate (DEF; Sigma Ltd, UK), an esterase

specific inhibitor.

N. Abbas et al.

123

Concentration response bioassays

A feeding bioassay method was used to determine the tox-

icity of the five above mentioned insecticides (Kaufman et al.

2006). A range of five serial solutions (causing [0 % and

\100 % mortalities) were prepared. Following Marcon et al.

(2003), ten 2-3-day-old randomly collected male and female

flies were placed into plastic jars (500 ml) and provided one

piece of cotton dental wick (3 cm length) moistened with

20 % sugar water solution containing different concentra-

tions of insecticides. Five concentrations were prepared as

serial dilutions for each insecticide and each concentration

was replicated three times (30 flies for each concentration of

total three replications). In control plastic jars, cotton wicks

soaked in 20 % sugar solution without insecticide were

provided to flies (n = 30 flies). To avoid drying, cotton

wicks were hydrated (without sugar solution) at 24 and 48 h

(Kaufman et al. 2006; Khan et al. 2013a, c). All the flies were

kept under the same conditions as described in section

‘‘Insects’’. Mortality was assessed 48 h after treatment to

lambda-cyhalothrin, bifenthrin, methomyl due to fast acting

nature and 72 h after treatment to abamectin and indoxacarb

due to slow acting nature. All ataxic flies were assumed dead.

Population selection with lambda-cyhalothrin

The population collected from the poultry farm, designated as

Field Pop. was split into two sub-populations after the 1st

generation (G1), one of which was exposed to the insecticide

and designated as Lambda-SEL and the other to control

conditions designated as UNSEL. Selection of Lambda-SEL

was performed for 11 successive generations. Before starting

the selection, the field collected flies were bioassayed (5–6

concentrations) to determine the lethal concentration for

desired selection process (i.e. 90 % mortality; 128 lg ml-1).

Two day old house flies were exposed to lambda-cyhalothrin

by providing cotton wicks soaked in 20 % sugar solution for

the selection experiment. Mortality was assessed 48 h after

treatment and the surviving flies were used as parents of the

next generation. The number of adult flies exposed in each

generation varied from 400 to 1,600 depending on survival

and availability of adult flies.

Synergism experiment

PBO or DEF was diluted in acetone (analytical reagent;

Fisher Scientific, Loughborough, UK) and mixed in serial

solutions containing insecticide doses. The highest non

lethal dose was used for the synergism experiment. For the

Lambda-SEL line, these concentrations were 5 mg ml-1

PBO and 10 mg ml-1 DEF, while for the susceptible line,

a concentration of 1 mg ml-1 was used for both com-

pounds. Acetone was used alone for control. Mortality was

assessed 48 h after the treatment.

Genetic crosses

To determine the inheritance of lambda-cyhalothrin resistance

in house flies, it was assumed that the Lambda-SEL and

Susceptible populations were homogeneously resistant and

susceptible, respectively (Tabashnik 1991). The male and

female adult flies were separated within 24 h from eclosion to

ensure virginity (Zhang et al. 2008). Sex determination was

based on the space between red compound eyes, (i.e. larger in

female and smaller in male). For the F1 cross population, 10

Lambda-SEL male flies were crossed with 10 Susceptible

female flies and for the F0

1 cross population, 10 Lambda-SEL

female flies were crossed with 10 Susceptible male flies to

produce the next progeny. The F2 population was obtained by

self crossing the F1 population. Backcross progeny was pro-

duced from four backcross lines: BC1 (F1 $ 9 Susceptible #),

BC2 (F01 $ 9 Susceptible #), BC3 (F1 $ 9 Lambda-SEL #)

and BC4 (F01 $ 9 Lambda-SEL #).

Realized heritability (h2)

The realized heritability (h2) was estimated according to

Falconer (1989) and Tabashnik (1992).

h2 = Response to selection Rð Þ=Selection differential (S)

Selection response was calculated as follows:

R = Log final LC50- Log Initial LC50ð Þ= N

Here, the final LC50 is the population’s LC50 after 11

generations of selection, initial LC50 is the LC50 of parental

population before selection and N is the number of gen-

erations submitted to selection by lambda-cyhalothrin.

Selection differential was calculated as follows:

S = i� rp

Where i is the intensity of selection calculated according

to Falconer (1989), rp is the phenotypic standard deviation

as calculated from:

rp = initial slope + final slopeð Þ0:5½ ��1

Based on the response of house flies to selection in the

laboratory, the number of generations required for a tenfold

increase in LC50 (G) was calculated as:

G = R�1

Resistance of the house fly Musca domestica (Diptera: Muscidae) to lambda-cyhalothrin

123

Data analysis

Concentration response bioassays

The concentration response data were analysed by probit

analysis (Finney 1971) with POLO software (LeOra Soft-

ware 2005), to determine LC50 mean values, standard

errors, slopes and 95 % confidence intervals (CIs). Control

mortality was corrected by using Abbott’s formula (Abbott

1925) if occured. The resistance ratio (RR) was determined

as the LC50 of Lambda-SEL population divided by the

LC50 of the Susceptible population. LC50 values of F1

populations were considered as non significantly different

(P [ 0.05) when their CIs overlapped (Litchfield and

Wilcoxon 1949).

Degree of dominance

The dominance (DLC) value of lambda-cyhalothrin resis-

tance was determined according to Stone (1968) and

Bourguet and Raymond (1998) while effective dominance

(DML) was estimated according to Bourguet et al. (2000)

and Basit et al. (2011) using the following formula:

DML¼ MTRS �MTSSð Þ= MTRR �MTSSð Þ

Where MTRR, MTRS, and MTSS were the percent mor-

talities to a single insecticide dose for the Lambda-SEL, F1

and Susceptible populations, respectively. DML increases

with the level of dominance, and varies from 0 to 1, i.e.,

complete recessivity to complete dominance.

Number of factors involved

The number of genetic factors involved in the observed

resistance was estimated using two approaches. First, the

hypothesis of monogenic resistance was tested statistically

using a chisquare goodness of fit test. According to Sokal

and Rohlf (1981) the null hypothesis of monogenic resis-

tance was calculated using the following formula:

v2 = (Ni� pni)2= pqni

Where Ni is the observed mortality in BC3 population

against a particular dose, ni is the number of individuals

exposed to a particular dose, p is the expected mortality

calculated according to Georghiou (1969) and q is calcu-

lated as 1-p. The null hypothesis of monogenic resistance

was rejected when the mortality observed in BC3 was

significantly different from that expected.

Secondly, the amount of genes controlling lambda-cy-

halothrin resistance was calculated according to Lande

(1981) method using the following formula:

gE = XRR � XSSð Þ2= 8r2S� �

Where XRR and XSS were the log LC50 values of

Lambda-SEL and Susceptible populations, respectively,

and r2S was estimated as follows:

r2s = r2B1þr2

B2 � r2F1þ0:5r2XSSþ0:5r2XRR

� �

Where r2B1, r2

B2, r2F1, r2XSS and r2XRR were the

variances of the BC1, BC3, F1, Susceptible and Lambda-

SEL populations, respectively. Variance was calculated

according to Lande (1981) method as inverse of the

squared slope (standard deviation).

Results

Effect of different insecticides on the Susceptible, field,

UNSEL and Lambda-SEL populations of house fly

Lambda-cyhalothrin, bifenthrin and methomyl were equally

toxic to the Susceptible population, and less toxic than ind-

oxacarb and abamectin. However, abamectin was the most

toxic insecticide against the Susceptible population

(Table 1). Lambda-cyhalothrin, bifenthrin, indoxacarb and

methomyl were significantly less toxic to the field population

than to the susceptible population and led to a RR of 9.27-

fold, 11.15-fold, 4.52-fold and 3.73-fold, respectively. The

abamectin was not significantly less toxic to the field popu-

lation than to the susceptible population (Table 1).

Lambda-cyhalothrin, bifenthrin and indoxacarb were sig-

nificantly less toxic to the UNSEL population than to the

susceptible population and led to a RR of 2.39-fold, 4.27-fold

and 2.99-fold, respectively. Methomyl and abamectin were

not significantly less toxic to the field population than to the

susceptible population. All tested insecticides were signifi-

cantly less toxic to the Lambda-SEL population than to the

Susceptible one. After 11 generations of selection, the

Lambda-SEL population developed a RR of 113.57-fold and

12.25-fold compared with the Susceptible and field popula-

tions (Table 1). The average mortality of flies exposed to

lambda-cyhalothrin at different selection concentrations after

48 h of exposure was 75 %.

Cross-resistance to different insecticides

in the Lambda-SEL population

The Lambda-SEL population at G11 was used to assess the

cross-resistance against different insecticides. Results

indicated that the selection imposed by lambda-cyhalothrin

induced a 3.93-fold and 3.98-fold increase in resistance to

indoxacarb and abamectin compared to the poultry farm

field population, respectively. However, lambda-cyhaloth-

rin selection did not increase the resistance against

N. Abbas et al.

123

bifenthrin and methomyl (95 % CIs overlap; Table 1). The

Lambda-SEL population showed very low cross-resistance

against indoxacarb and abamectin and a lack of cross-

resistance to bifenthrin and methomyl.

Effect of PBO and DEF on insecticide toxicity

The enzyme inhibitors PBO and DEF interacted synergis-

tically with all tested insecticides (Table 2). PBO and DEF

had a potentiating effect on lambda-cyhalothrin but neither

on indoxacarb nor abamectin in the susceptible population.

PBO significantly reduced LC50 values (95 % CI did not

overlap) for lambda-cyhalothrin from 568.51 to 34.13

(16.66-fold), indoxacarb from 48.69 to 12.06 (4.04-fold)

and abamectin from 3.75 to 0.83 (4.52 fold) in the Lambda-

SEL population. DEF also reduced LC50 values for

lambda-cyhalothrin from 568.51 to 275.76 (2.06-fold),

indoxacarb from 48.69 to 9.51 (5.12-fold) and abamectin

from 3.75 to 0.88 (4.26 fold) in the Lambda-SEL

population.

Degree of dominance and sex linkage

The dominance (DLC) values were 0.68, 0.62, and 0.67 for

the F1, F01 and F2 populations, respectively (Table 3)

indicating incompletely dominant inheritance of resistance

against lambda-cyhalothrin in the studied lines. The results

for effective dominance (DML) indicate that the level of

dominance decreased when the lambda-cyhalothrin dose

increased from 32 to 512 lg ml-1 (Table 4). Resistance

was completely dominant at the lowest concentration

(DML = 0.950) and completely recessive at highest con-

centration (DML = 0.000).

The RR for lambda-cyhalothrin was 113.57-fold in the

Lambda-SEL population compared to the Susceptible

population (Table 3). Compared to the Susceptible popu-

lation, lines from reciprocal crosses exhibited higher

resistance ratios, i.e., 25.55 and 18.98 fold in F1 and F01lines, respectively. The LC50 of reciprocal cross popula-

tions did not differ significantly from each other (see CI

overlap), suggesting that in the studied populations,

Table 1 Toxicity of different insecticides on the susceptible, field, UNSEL and Lambda-SEL (G11) populations of house fly

Populations Insecticides LC50 [95 % CI] (lg ml-1) Slope (± SE) v2 Df P na RRb RRc

Susceptible (G14) Lambda-cyhalothrin 4.97 (3.37–7.33) 1.74 ± 0.35 1.03 4 0.91 140

Susceptible (G14) Bifenthrin 10.52 (5.92–15.99) 1.47 ± 0.34 1.17 4 0.88 120

Susceptible (G14) Methomyl 5.90 (4.38–7.76) 2.59 ± 0.44 1.14 4 0.89 120

Susceptible (G14) Indoxacarb 1.41 (0.92–2.01) 1.81 ± 0.36 1.54 4 0.82 120

Susceptible (G14) Abamectin 0.46 (0.33–0.65) 2.59 ± 0.51 1.44 4 0.84 120

Field Pop. (G1) Lambda-cyhalothrin 46.07 (35.01–59.50) 2.89 ± 0.48 0.72 4 0.95 120 9.27

Field Pop. (G1) Bifenthrin 117.36 (89.22–163.62) 2.00 ± 0.38 2.24 3 0.52 120 11.15

Field Pop. (G1) Methomyl 22.03 (16.19–28.99) 2.56 ± 0.44 0.81 4 0.94 120 3.73

Field Pop. (G1) Indoxacarb 6.37 (3.31–24.76) 1.12 ± 0.39 2.37 4 0.67 120 4.52

Field Pop. (G1) Abamectin 1.25 (0.62–1.98) 1.32 ± 0.33 1.49 4 0.83 120 2.72

UNSEL (G11) Lambda-cyhalothrin 11.86 (8.03–15.53) 2.26 ± 0.39 1.36 4 0.85 180 2.39

UNSEL (G11) Bifenthrin 44.89 (32.16–60.15) 2.33 ± 0.41 1.97 4 0.74 120 4.27

UNSEL (G11) Methomyl 8.73 (5.806–13.451) 1.61 ± 0.34 0.56 4 0.97 120 1.48

UNSEL (G11) Indoxacarb 4.22 (2.57–6.00) 1.85 ± 0.38 1.94 4 0.75 120 2.99

UNSEL (G11) Abamectin 0.84 (0.62–1.25) 2.11 ± 0.40 1.71 4 0.79 120 1.83

Lambda-SEL (G11) Lambda-cyhalothrin 564.48 (416.14–774.45) 2.26 ± 0.39 1.99 4 0.74 120 113.57 12.25

Lambda-SEL (G11) Bifenthrin 203.91 (150.17–296.49) 2.11 ± 0.38 0.02 4 1 120 19.38 1.74

Lambda-SEL (G11) Methomyl 22.74 (16.90–29.77) 2.65 ± 0.45 1.72 4 0.79 120 3.85 2.6

Lambda-SEL (G11) Indoxacarb 25.04 (17.90–38.18) 1.93 ± 0.37 0.29 4 0.99 120 17.75 3.93

Lambda-SEL (G11) Abamectin 4.97 (3.46–6.70) 2.26 ± 0.41 2.94 4 0.57 120 5.91 3.98

P values are calculated on the basis of Chi square goodness of fit test

P [ 0.05 does not show goodness of fit, it reflects the lack of fit to H0a n Number of adults flies used in bioassay, including controlsb RR resistance ratio, calculated as (LC50 of field, UNSEL and Lambda-SEL population)/(LC50 of Susceptible population)c RR resistance ratio, calculated as (LC50 of Lambda-SEL population)/(LC50 of field population)

Resistance of the house fly Musca domestica (Diptera: Muscidae) to lambda-cyhalothrin

123

resistance to lambda-cyhalothrin is autosomal (no sex

linkage) and not affected by maternal effects (Table 3).

Number of factors involved

The test for monogenic resistance indicated significant

departure from expectations, under four concentrations

(Table S1). This strongly suggests that resistance to

lambda-cyhalothrin is controlled by multiple factors.

Similarly, the number of genes controlling resistance was

[3. These results provided evidence that lambda-cyhal-

othrin resistance was controlled by multiple genes in the

Lambda-SEL population.

Table 2 Toxicity of different insecticides alone and with PBO or DEF to susceptible and Lambda-SEL populations of house fly

Populations Insecticides LC50 (95 % CI) Slope (± SE) v2 Df P RR SR

Susceptible (G27) Lambda-cyhalothrin 1.94 (1.38–2.53) 2.11 ± 0.34 0.76 4 0.94 –

Susceptible(G27) Lambda-cyhalothrin ? PBO 0.27 (0.01–0.57) 0.78 ± 0.28 2.24 4 0.69 7.18

Susceptible (G27) Lambda-cyhalothrin ? DEF 0.65 (0.27–1.12) 0.99 ± 0.28 5.35 4 0.25 2.98

Susceptible (G27) Indoxacarb 0.35 (0.19–0.51) 1.60 ± 0.31 3.23 4 0.52 –

Susceptible (G27) Indoxacarb ? PBO 0.32 (0.21–0.44) 1.74 ± 0.32 2.21 4 0.70 1

Susceptible (G27) Indoxacarb ? DEF 0.49 (0.33–0.72) 1.54 ± 0.30 1.15 4 0.89 0.71

Susceptible (G27) Abamectin 0.24 (0.12–0.35) 1.29 ± 0.27 4.52 4 0.34 –

Susceptible (G27) Abamectin ?PBO 0.26 (0.19–0.34) 2.32 ± 0.39 2.06 4 0.73 0.92

Susceptible (G27) Abamectin ?DEF 0.23 (0.13–0.34) 1.58 ± 0.32 0.11 4 1.00 1

Lambda-SEL (G21) Lambda-cyhalothrin 568.51 (461.67–702.60) 2.88 ± 0.38 5.87 4 0.21 293.04 –

Lambda-SEL (G21) Lambda-cyhalothrin ? PBO 34.13 (19.49–130.28) 1.14 ± 0.29 0.83 4 0.93 126.41 16.66

Lambda-SEL (G21) Lambda-cyhalothrin ? DEF 275.76 (178.07–379.41) 1.62 ± 0.29 7.02 4 0.13 424.24 2.06

Lambda-SEL (G21) Indoxacarb 48.69 (37.71–71.55) 2.56 ± 0.46 1.78 4 0.78 139.11 –

Lambda-SEL (G21) Indoxacarb ?PBO 12.06 (9.58–15.47) 2.94 ± 0.45 6.37 4 0.17 37.69 4.04

Lambda-SEL (G21) Indoxacarb ?DEF 9.51 (6.77–12.51) 1.93 ± 0.31 1.19 4 0.88 19.41 5.12

Lambda-SEL (G21) Abamectin 3.75 (2.67–5.20) 1.60 ± 0.28 0.53 4 0.97 15.62 –

Lambda-SEL (G21) Abamectin ?PBO 0.83 (0.61–1.11) 2.12 ± 0.35 4.02 4 0.40 3.19 4.52

Lambda-SEL (G21) Abamectin ?DEF 0.88 (0.60–1.17) 2.03 ± 0.34 0.52 4 0.97 3.83 4.26

RR Resistance ratio calculated as LC50 of Lambda-SEL/LC50 of Susceptible

SR Synergism ratio calculated as LC50 of insecticide alone/LC50 of insecticide ? PBO or of insecticide ? DEF

P values are calculated on the basis of Chi square goodness of fit test

P [ 0.05 does not show goodness of fit, it reflects the lack of fit to H0

Table 3 Response of lambda-cyhalothrin to the susceptible, Lambda-SEL, F1 (both reciprocal crosses), F2 and all backcrossed populations of

house fly

Populations LC50 (95 % CI) (lg ml-1) Slope (± SE) v2 df P N RR DLC r2DLC

Susceptible (G14) 4.97 (3.367–7.326) 1.74 ± 0.35 1.03 4 0.91 120 1 –

Lambda-SEL (G11) 564.48 (416.14–774.45) 2.26 ± 0.39 1.99 4 0.74 120 113.57 –

F1 (Lambda-SEL $ 9 Susceptible #) 127.24 (86.19–187.55) 1.74 ± 0.35 1.03 4 0.91 120 25.55 0.68 0.03

F01 (Lambda-SEL # 9 Susceptible $) 94.36 (60.63–136.33) 1.73 ± 0.35 1.70 4 0.79 120 18.98 0.62 0.03

F2 (F1 $ 9 F1 #) 120.31 (90.74–158.44) 1.95 ± 0.29 4.64 4 0.33 120 24.20 0.67 0.02

BC1 (F1 $ 9 Susceptible #) 21.31 (12.80–31.43) 1.60 ± 0.34 0.45 4 0.98 140 4.28 –

BC2 (F01 $ 9 Susceptible #) 32.12 (20.74–49.79) 1.54 ± 0.33 0.29 4 0.99 140 6.46 –

BC3 (F1 $ 9 Lambda-SEL #) 148.95 (114.39–195.77) 2.55 ± 0.40 1.59 4 0.81 142 29.97 –

BC4 (F01 $ 9 Lambda-SEL #) 246.84 (158.87–378.76) 1.23 ± 0.26 0.53 4 0.97 180 49.66 –

RR Resistance ratio is determined as LC50 of the Lambda-SEL or F1 (reciprocal) or backcross populations/LC50 of the susceptible

DLC degree of resistance dominance, ranged 0 completely recessive, and 1 completely dominant

P values are calculated on the basis of Chi square goodness of fit test

P [ 0.05 does not show goodness of fit, it reflects the lack of fit to H0

N. Abbas et al.

123

Realized heritability (h2)

After 11 generations of selection with lambda-cyhalothrin, the

LC50 of the Lambda-SEL population of house fly increased

from 46.07 to 564.48 lg ml-1 and the slope decreased from

2.89 to 2.26. The heritability values were 0.20, 0.04, 0.003,

0.07 and 0.08 for cross-resistance to lambda-cyhalothrin,

bifenthrin, methomyl, indoxacarb and abamectin, respec-

tively. The number of generations required for a tenfold

increase in LC50 of lambda-cyhalothrin, bifenthrin, meth-

omyl, indoxacarb and abamectin were expected to be 100, 50,

1,000, 20 and 20, respectively (reciprocal of R; Table S2).

Discussion

Lambda-cyhalothrin is widely used for the control of house

fly (see introduction). Consistently, before selection in the

laboratory, the poultry farm population used in the present

study already exhibited a ninefold resistance to this

insecticide. Furthermore, after a 11 generation experi-

mental exposure, the selected line developed a dramatic

increase in resistance (more than 100-fold) compared to the

susceptible one. Resistance has been previously reported in

house fly against various insecticides (Scott et al. 2000;

Kaufman et al. 2001, 2006, 2010; Shono et al. 2002, 2004;

Zhang et al. 2008; Acevedo et al. 2009; Shi et al. 2011;

Khan et al. 2013a, c). The slope of the mortality curve did

not differ significantly between the field (G1) and Lambda-

SEL (G11) populations. According to Ahmad et al. (2007)

non-significant difference between selected and non

selected populations indicates low genetic variation with

respect to expression of insecticide resistance. Indeed,

phenotypic deviation in susceptibility is reflected by the

slope of the mortality curve (Hoskins 1960). However, as it

is contributed by both genetic and environmental variance

(VE), the change in slope is not a good indicator of genetic

variation in susceptibility (Chilcutt and Tabashnik 1995).

Cross-resistance

Cross-resistance has been assumed a valuable tool in

assessing insecticide resistance mechanisms (Khan et al.

2014). In the present study, no cross-resistance to bif-

enthrin and to methomyl was detected, and cross-resistance

to indoxacarb and abamectin was low. Regarding lambda-

cyhalothrin and bifenthrin, the result is not in line with

what may be expected with molecules of the same insec-

ticide class, and indicates independent mechanisms (see

Khan et al. 2014). In terms of control strategy, this result is

interesting as it suggests that lambda-cyhalothrin and bif-

enthrin can be used in rotation in the field, which will

reduce the selection pressure of a specific product and

ultimately delay the development of resistance to both

products. Previously, it has been reported that a delta-

methrin selected population of S. litura showed low cross-

resistance against cypermethrin (17-fold) and no cross-

resistance against organophosphate insecticides. Similarly,

a deltamethrin selected population of P. xylostella showed

low cross-resistance against spinosad (tenfold), and no

cross-resistance against fipronil (onefold) and indoxacarb

(twofold) (Sayyed et al. 2005). In house flies, a permethrin

selected population showed cross-resistance to fipronil,

imidacloprid and chlorpyrifos (Liu and Yue 2000). In the

present study, weak resistance, or lack thereof, between

lambda-cyhalothrin and the four tested insecticides sug-

gests the possibility of efficient rotational use involving

these molecules.

Consistent with previous results on house fly resistance

to pyrethroids (Scott and Georghiou 1985; Scott 1999;

Shono et al. 2002; Kristensen et al. 2004), the synergistic

effects observed between enzyme inhibitors PBO and DEF

and lambda-cyhalothrin indicate a major role of CYP450

and esterases in the mechanisms underlying resistance in

the selected lines. As a consequence, cross-resistance with

other insecticides is likely, due to the occurrence of these

Table 4 Effective dominance (DML) of resistance to lambda-cyhal-

othrin in the lambda-SEL population of house fly according to

insecticide dose

Dose

(lg ml-1)

Population Mortality

(%)

DMLa

32 Susceptible 100 0.95

Lambda-

SEL

0 Completely dominant

Pooled F1 4.55

64 Susceptible 100 0.77

Lambda-

SEL

0 Incompletely

dominant

Pooled F1 22.73

128 Susceptible 100 0.70

Lambda-

SEL

9.09 Incompletely

dominant

Pooled F1 36.36

256 Susceptible 100 0.41

Lambda-

SEL

22.73 Incompletely

recessive

Pooled F1 68.18

512 Susceptible 100 0.00

Lambda-

SEL

31.82 Completely recessive

Pooled F1 100

Numbers of flies per dose were 22 for the susceptible, Lambda-SEL

and F1 populationsa DML Effective dominance of resistance, ranged from 0 (completely

recessive) to 1 (completely dominant)

Resistance of the house fly Musca domestica (Diptera: Muscidae) to lambda-cyhalothrin

123

enzymes under various isoforms (Ishaaya and Casida

1981). The fact that our results do not support this

hypothesis (no or weak cross-resistance) may reflect spe-

cific properties of the selected pesticides, yet it does not

preclude the possibility of cross-resistance with other

molecules.

Mono vs polygenic resistance

The present experiment indicated autosomal and polygenic

resistance to lambda-cyhalothrin. Similarly, house fly

resistance to permethrin was found as incompletely reces-

sive and polygenic (Liu and Scott 1995; Liu and Yue 2001;

Shono et al. 2002), whereas resistance to beta-cypermeth-

rin appears monogenic (Zhang et al. 2008). In the latter

case however, autosomal inheritance and incomplete re-

cessivity was observed, as for lambda-cyhalothrin. With

regard to resistance to another pyrethroid, deltamethrin, our

results are consistent with those obtained from other insects

(P. xylostella, Sayyed et al. 2005; S. litura, Ahmad et al.

2007).

Polygenic and monogenic resistance may occur in nat-

ural populations. However, the monogenic resistance is less

likely under laboratory selection, due to the absence of rare

variants that may be present in large natural populations

(Roush and Mckenzie 1987; Mckenzie et al. 1992; Yuan

et al. 2007). Consistently, our results showed a polygenic

basis for the resistance to lambda-cyhalothrin. Sayyed and

Wright (2001) found that the resistance controlled by

multiple genes, has been evenly spread between the labo-

ratory and field selected populations. Succession of dif-

ferent mechanisms, and of different resistant alleles at a

given locus, may occur through time, which precludes

resistance to be considered as a stable state, once estab-

lished in a population. It could be due to major and minor

genes in the laboratory and field selected resistance (Gro-

eters and Tabashnik 2000), although major genes will be

likely to respond more rapidly to selection pressure than

minor genes. The different selection histories in the field

may result in the polygenic genetic basis of pyrethroid

resistance.

Dominance

The genetic basis of resistance to pyrethroids including

lambda-cyhalothrin has been studied in several insect pests

(e.g., Zhang et al. 2008). Although in most of the studies,

the resistance was inherited as an autosomal, and incom-

pletely dominant to incompletely recessive trait (Liu and

Yue 2001; Sayyed et al. 2005), differences exist in terms of

inheritance pattern (autosomal vs sex linked) and number

of genes involved. For instance, permethrin resistance in

the horn fly was inherited as a single, recessive, sex-linked

gene (McDonald and Schmidt 1987), whereas an autoso-

mal multigenic, and incompletely recessive trait was

involved in the house fly (Liu and Yue 2001). In contrast,

autosomal multigenic and incompletely dominant traits

were involved in resistance to deltamethrin in P. xylostella,

a vegetable pest (Sayyed et al. 2005), and it was assumed

that recessive or dominant expression of the resistance

depended upon the concentrations of deltamethrin to which

the pest had been exposed. These differences might be due

to variation in environmental conditions and insecticide

exposure to the insect pests in the field (Bourguet et al.

2000). In the present study, resistance to lambda-cyhal-

othrin was found incompletely dominant in the selected

lines of house fly. In addition, the degree of dominance was

dependent on the concentrations tested i.e., completely

dominant at the lowest dose tested and vice versa. Phe-

notypic expression of insecticide resistance could be due to

a single locus with major effect, for example, a single gene

responsible for the overexpression of a detoxifying

enzyme, or it could be due to the additive effect of multiple

loci (ffrench-Constant 2013; ffrench-Constant et al. 2004).

The results revealed that the resistance to lambda-cyhal-

othrin in Lambda-SEL strain segregates in a multifactor

fashion, as already reported for resistance to other pyre-

throids (Liu and Yue 2001; Sayyed et al. 2005, 2010).

Susceptible alleles, if recessive, might be maintained

longer in the population exposed to the selection pressure,

because they are masked in heterozygotes (as compared to

codominance or dominance), which tends to slow down

fixation of the resistant allele, despite its selective

advantage (Ferre and Van Rie 2002). Likewise, interac-

tions between major and minor genes can contribute to

maintain sensitive alleles in populations (Sayyed et al.

2000). The present results showed that differences in the

response to laboratory and field selection is mainly based

on the extant of genetic variation, but population struc-

ture, environmental variation and differing selection

intensities can also cause discrepancies between lab and

field responses.

Realized heritability

Phenotypic variation (VP) is contributed by genetic and

environmental factors (Yang 2000). Falconer (1989)

defines h2 as the proportion of VP accounted for by addi-

tive genetic variation (VA), which may decrease either due

to the decrease in VA or to the increase in VE. In the

present study, the maintain of high h2 after 11 generations

of selection with lambda-cyhalothrin indicated that house

flies may have higher chances to develop resistance to

lambda-cyhalothrin than to spinosad (h2 = 0.14, Shi et al.

N. Abbas et al.

123

2011) and to imidacloprid (h2 = 0.10, Li et al. 2012). The

present results are similar to those obtained with beta-cy-

permethrin (h2 = 0.30, Zhang et al. 2008). The most likely

explanation for the maintenance of high heritability is that

h2 is artificially inflated by the decrease in VE, as expected

from the field to the laboratory (Posthuma et al. 1993;

Klerks et al. 2011). The number of generations necessary

for tenfold increase in LC50 of the Lambda-SEL population

was expected to be 100 generations if the population was

continuously exposed to lambda-cyhalothrin. Although it is

clear that laboratory experiments do not reflect field con-

ditions, h2 estimated in the laboratory provides useful

information on the potential for resistance increase in

house fly (Tabashnik 1992).

Knowledge of the mode of inheritance characterizing

insecticide resistance, as based on laboratory experiments,

is necessary for the sustainability of biological control and

pest management (Bouvier et al. 2001; Zhang et al. 2008).

A systematic and comprehensive strategy is necessary for

delaying the development of resistance. Some management

strategies (e.g. high-dose strategy) are very effective

against recessive mode of inheritance (Roush and Daly

1990). The strategies such as responsive alternation,

mosaic, periodic application and combinations may delay

the development of resistance (REX consortium, 2013).

Resistance could be changed because it is a spatial and

temporal phenomenon (Zhao et al. 2006). In the present

study, lack of cross-resistance between lambda-cyhalothrin

and other compounds such as bifenthrin and methomyl, and

very low cross-resistance between lambda-cyhalothrin and

new chemicals such as indoxacarb and abamectin indicates

that the above mentioned insecticides, which are used for

the management of house flies worldwide (Geden et al.

1990; Kaufman et al. 2001; Shono et al. 2004) could be

rotated as alternatives to decrease lambda-cyhalothrin

selection in poultry farms in Pakistan. In rotations, the use

of an insecticide will be limited for a short time to delay the

development of resistance and the efficacy of new chemi-

cals will be sustained for long term by optimizing their use.

Therefore, identification and monitoring of resistant genes

in house fly field populations will be essential for the

management of resistance development. In this context,

results from the present study provide relevant information

for the house fly control.

Acknowledgments We are highly thankful to Dr. Abdul Waheed,

Lecturer, Faculty of Veterinary Sciences, Bahauddin Zakariya Uni-

versity Multan, Pakistan for technical assistance. We also indebted to

Muhammad Ismail, Technical Development Officer, Syngenta

(Pakistan) Limited for sparing time to visit poultry farms for insect

collection.

Conflict of interests The authors declare that they have no com-

peting interests.

References

Abbott WS (1925) A method of computing the effectiveness of an

insecticide. J Econ Entomol 18:265–267

Abou-Yousef HM, Farghaly SF, Singab M, Ghoneim YF (2010)

Resistance to lambda-cyhalothrin in laboratory strain of whitefly

Bemisea tabaci (Genn.) and cross resistance to several insecti-

cides. Am-Eurasian J Agric Environ Sci 7:693–696

Acevedo GR, Zapater M, Toloza AC (2009) Insecticide resistance of

house fly, Musca domestica (L.) from Argentina. Parasitol Res

105:489–493

Achaleke J, Brevault T (2010) Inheritance and stability of pyrethroid

resistance in the cotton bollworm Helicoverpa armigera (Lep-

idoptera: Noctuidae) in Central Africa. Pest Manag Sci

66:137–141

Ahmad M, Sayyed AH, Crickmore N, Saleem MA (2007) Genetics

and mechanism of resistance to deltamethrin in a field population

of Spodoptera litura (Lepidoptera: Noctuidae). Pest Manag Sci

63:1002–1010

Aizoun N, Aıkpon R, Padonou GG, Oussou O, Oke-Agbo F,

Gnanguenon V, Osse R, Akogbeto M (2013) Mixed-function

oxidases and esterases associated with permethrin, deltamethrin

and bendiocarb resistance in Anopheles gambiae s.l. in the

south-north transect Benin West Africa. Parasit Vectors

6:223–233

Axtell RC (1985) Arthropod pests of poultry. In: Williams RE, Hall

RD, Bruce AB, Scholl PJ (eds) Livestock Entomology. Wiley,

New York, pp 269–296

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

Prot 30:705–712

Bass C, Linda MF (2011) Gene amplification and insecticide

resistance. Pest Manag Sci 67:886–890

Bourguet D, Genissel A, Raymond M (2000) Insecticide resistance

and dominance levels. J Econ Entomol 93:1588–1595

Bourguet D, Raymond M (1998) The molecular basis of dominance

relationships: the case of some recent adaptive genes. J Evol Biol

11:103–122

Bouvier JC, Bues R, Boivin T, Boudinhon L, Beslay D, Sauphanor B

(2001) Deltamethrin resistance in codling moth: inheritance and

number of genes involved. Heredity 87:456–462

Chilcutt CF, Tabashnik BE (1995) Evaluation of pesticide resistance

and slope of the concentration-mortality line: are they related?

J Econ Entomol 88:11–20

Devonshire AL (1973) The biochemical mechanisms of resistance to

insecticides with special reference to the housefly, Musca

domestica and aphid, Myzus persicae. Pest Manag Sci 4:521–529

Falconer DS (1989) Introduction to quantitative genetics. Longman,

London

Ferre J, Van Rie J (2002) Biochemistry and genetics of insect

resistance to Bacillus thuringiensis. Annu Rev Entomol

47:501–533

ffrench-Constant RH (2013) The molecular genetics of insecticide

resistance. Genetics 194:807–815

ffrench-Constant RH, Daborn PJ, Goff GL (2004) The genetics and

genomics of insecticide resistance. Trends Genet 20:163–170

Finney DJ (1971) Probit analysis, 3rd edn. Cambridge University

Press, Cambridge

Forster M, Klimpel S, Mehlhorn H, Sievert K, Messler S, Pfeffer K

(2007) Pilot studies on synantropic flies (e.g. Musca, Sarcoph-

aga, Calliphora, Fania, Lucilia, Stomoxys) as vectors of

pathogenic microorganisms. Parasitol Res 101:243–246

Geden CJ, Steinkraus DC, Long SJ, Rutz DA, Shoop WL (1990)

Susceptibility of insecticide-susceptible and wild house flies

Resistance of the house fly Musca domestica (Diptera: Muscidae) to lambda-cyhalothrin

123

(Diptera: Muscidae) to abamectin on whitewashed and unpainted

wood. J Econ Entomol 83:1935–1939

Georghiou GP (1969) Genetics of resistance to insecticides in house

flies and mosquitoes. Exp Parasitol 26:224–255

Gregory TP, Robert GB, Thomas MB (1988) Inheritance of

permethrin resistance in the tobacco budworm (Lepidoptera:

Noctuidae). J Econ Entomol 81:65–73

Groeters FR, Tabashnik BE (2000) Roles of selection intensity, major

genes, and minor genes in evolution of insecticide resistance.

J Econ Entomol 93:1580–1587

Hoskins WM (1960) Use of the dosage mortality curve in quantitative

estimation of insecticide resistance. Entomol Soc Am 2:85–91

Ishaaya I, Casida JE (1981) Pyrethroid esterase(s) may contribute to

natural pyrethroid tolerance of larvae of the common green

lacewing. Environ Entomol 10:681–684

Kaufman PE, Gerry AC, Rutz DA, Scott JG (2006) Monitoring

susceptibility of house flies (Musca domestica L.) in the United

States to imidacloprid. J Agric Urban Entomol 23:195–200

Kaufman PE, Nunez SC, Mann RS, Christopher GJ, Scharfa E (2010)

Nicotinoid and pyrethroid insecticide resistance in house flies

(Diptera: Muscidae) collected from Florida dairies. Pest Manag

Sci 66:290–294

Kaufman PE, Scott JG, Rutz DA (2001) Monitoring insecticide

resistance in house flies (Diptera: Muscidae) from New York

dairies. Pest Manag Sci 57:514–521

Khan HAA, Akram W, Shad SA (2014) Genetics, cross resistance and

mechanism of resistance to spinosad in a resistant strain of Musca

domestica L. (Diptera: Muscidae). Acta Trop 130:148–154

Khan HAA, Akram W, Shad SA (2013a) Resistance to conventional

insecticides in Pakistani populations of Musca domestica L.

(Diptera: Muscidae): a potential ectoparasite of dairy animals.

Ecotoxicol 22:522–527

Khan HAA, Akram W, Shad SA, Razaq M, Naeem-Ullah U, Zia K

(2013b) A cross sectional survey of knowledge, attitude and

practices related to house flies among dairy farmers in Punjab

Pakistan. J Ethnobiol Ethnomed 9:18

Khan HAA, Shad SA, Akram W (2013c) Resistance to new chemical

insecticides in the house fly Musca domestica L., from dairies in

Punjab Pakistan. Parasitol Res 112:2049–2054

Klerks PL, Xie L, Levinton JS (2011) Quantitative genetics

approaches to study evolutionary processes in ecotoxicology; a

perspective from research on the evolution of resistance.

Ecotoxicol 20:513–523

Kristensen M, Jespersen JB, Knorr M (2004) Cross-resistance

potential of fipronil in Musca domestica. Pest Manag Sci

60:894–900

Lande R (1981) The minimum number of genes contributing to

quantitative variation between and within populations. Genetics

99:541–553

Li J, Wang Q, Zhang L, Gao X (2012) Characterization of

imidacloprid resistance in the housefly Musca domestica (Dip-

tera: Muscidae). Pestic Biochem Physiol 102:109–114

Litchfield JT, Wilcoxon F (1949) A simplified method of evaluating

dose-effect experiments. J Pharmacol Exp Ther 99:99–103

Liu N, Yue X (2000) Insecticide resistance and cross-resistance in the

house fly (Diptera: Muscidae). J Econ Entomol 93:1269–1275

Liu NN, Scott JG (1995) Genetics of resistance to pyrethroid

insecticides in the house fly, Musca domestica. Pestic Biochem

Physiol 52:116–124

Liu NN, Yue X (2001) Genetics of pyrethroid resistance in a strain

(ALHF) of house flies (Diptera: Muscidae). Pestic Biochem

Physiol 70:151–158

Marcon PCRG, Thomas GD, Siegfried BD, Campbell JB, Skoda SR

(2003) Resistance status of house flies (Diptera: Muscidae) from

Southeastern Nebraska beef cattle feedlots to selected insecti-

cides. J Econ Entomol 96:1016–1020

McKenzie JA, Anthony G, Parker AG, Janet L, Yen JL (1992)

Polygenic and Single Gene Responses to Selection for Resis-

tance to Diazinon in Luciliacuprina. Genetics 130:613–620

McDonald PT, Schmidt CD (1987) Genetics of permethrin resistance

in the horn fly (Diptera: Muscidae). J Econ Entomol 80:433–437

Narahashi T, Zhao X, Ikeda T, Nagata K, Yeh JZ (2007) Differential

actions of insecticides on target sites: basis for selective toxicity.

Hum Exp Toxicol 26:361–366

Nauen R, Elbert A, McCaffery A, Slater R, Sparks TC (2012) IRAC:

insecticide resistance, and mode of action classification of

insecticides. In: Kramer W, Schirmer U, Jeschke P, Witschel M

(eds) Modern Crop Protection Compounds, vol 1–3. Wiley-VCH

Verlag GmbH and Co. KGaA, Weinheim

Posthuma L, Hogervorst RF, Joosse ENG, Van Straalen NM (1993)

Genetic variation and covariation for characteristics associated

with cadmium tolerance in natural populations of the springtail

Orchesella cincta (L.). Evolution 47:619–631

REX consortium (2013) Heterogeneity of selection and the evolution

of resistance. Trends Ecol Evol 28:110–118

Roush RT, Combs RL, Randolph TC, Macdonald J, Hawkins JA

(1986) Inheritance and effective dominance of pyrethroid

resistance in the horn fly (Diptera: Muscidae). J Econ Entomol

79:1178–1182

Roush RT, Daly JC (1990) The role of population genetics in

resistance research and management. In: Roush RT, Tabashnik

BE (eds) Pesticide Resistance in Arthropods. Chapman and Hall,

New York, pp 97–152

Roush RT, Mckenzie JA (1987) Ecological genetics of insecticide and

acaricide resistance. Annu Rev Entomol 32:361–380

Sayyed AH, Attique MNR, Khaliq A, Wright DJ (2005) Inheritance

of resistance to deltamethrin in Plutella xylostella (Lepidoptera:

Plutellidae) from Pakistan. Pest Manag Sci 61:636–642

Sayyed AH, Haward R, Herrero S, Ferre J, Wright DJ (2000) Genetic

and biochemical approach for characterisation of resistance to

Bacillus thuringiensis toxin Cry1Ac in a field population of the

diamondback moth. Appl Environ Microbiol 66:1509–1516

Sayyed AH, Wright DJ (2001) Cross-resistance and inheritance of

resistance Cry1Ac toxin in diamondback moth, Plutella xylo-

stella from lowland Malaysia. Pest Manag Sci 57:413–421

Sayyed AH, Pathan AK, Faheem U (2010) Cross-resistance, genetics

and stability of resistance to deltamethrinin a population of

Chrysoperla carnea from Multan, Pakistan. Pestic Biochem

Physiol 98:325–332

Scott JG (1999) Molecular basis of insecticide resistance: cyto-

chromes P450. Insect Bichem Mol Biol 29:757–777

Scott JG (2001) Cytochrome P450 monooxygenases and insecticide

resistance: lessons from CYP6D1. In: Ishaaya I (ed) Biochemical

Sites of Insecticide Action and Resistance. Springer, New York,

p 255

Scott JG, Alefantis TG, Kaufman PE, Rutz DA (2000) Insecticide

resistance in house flies from caged-layer poultry facilities. Pest

Manag Sci 56:147–153

Scott JG, Georghiou GP (1985) Rapid development of high-level

permethrin resistance in a field-collected strain of house fly

(Diptera: Muscidae) under laboratory selection. J Econ Entomol

78:316

Scott JG, Georghiou GP (1986) Mechanisms responsible for high

levels of permethrin resistance in the house fly. Pestic Sci 17:195

Shi J, Zhang L, Gao X (2011) Characterisation of spinosad resistance

in the house fly Musca domestica (Diptera:Muscidae). Pest

Manag Sci 67:335–340

Shono T, Kasai S, Kamiya E, Kono Y, Scott JG (2002) Genetics and

mechanisms of permethrin resistance in the YPER strain of

house fly. Pestic Biochem Physiol 73:27–36

Shono T, Zhang L, Scott JG (2004) Indoxacarb resistance in the house

fly, Musca domestica. Pestic Biochem Physiol 80:106–112

N. Abbas et al.

123

Soderlund DM, Knipple DC (2003) The molecular biology of

knockdown resistance to pyrethroid insecticides. Insect Biochem

Mol Biol 33:563–577

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

Petaluma

Sokal RR, Rohlf FJ (1981) Biometry. WH Freeman, San Francisco

Stone BF (1968) A formula determining degree of dominance in cases

of monofactorial inheritance of resistance to chemicals. Bull

WHO 38:325–326

Tabashnik BE (1991) Determining of the mode of inheritance of

pesticide resistance with backcross experiments. J Econ Entomol

84:703–712

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: Chrysome-

lidae). J Econ Entomol 85:1551–1559

Tian L, Cao C, He L, Li M, Zhang L, Zhang L, Liu H, Liu N (2011)

Autosomal interactions and mechanisms of pyrethroid resistance

in house flies, Musca domestica. Int J Biol Sci 7:902–911

Yang YH (2000) Basic Genetics. Higher Education Press, Beijing,

China, pp 264–299

Yuan JS, Tranel PJ, Stewart CN Jr (2007) Non-target-site herbicide

resistance: A family business. Trends Plant Sci 12:6–13

Zhang L, Shi J, Gao X (2008) Inheritance of beta-cypermethrin

resistance in the house fly Musca domestica (Diptera: Muscidae).

Pest Manag Sci 64:185–190

Zhao JZ, Collins HL, Li YX, Mau RFL, Thompson GD, Hertlein M,

Andaloro JT, Boykin R, Shelton AM (2006) Monitoring of

diamondback moth (Lepidoptera: Plutellidae) resistance to

spinosad, indoxacarb and emamectin benzoate. J Econ Entomol

99:176–181

Resistance of the house fly Musca domestica (Diptera: Muscidae) to lambda-cyhalothrin

123