Entomologia Experimentalis et Applicata 85: 169–175, 1997. 169c 1997 Kluwer Academic Publishers. Printed in Belgium.

Heritability of flight distance for Cydia pomonella

Peter Schumacher1, Donald C. Weber2, Christian Hagger3 & Silvia DornInstitute of Plant Sciences, Applied Entomology, Swiss Federal Institute of Technology (ETH), 8092 Zurich,Switzerland; 1Institute of Geobotany, Swiss Federal Institute of Technology (ETH), 8092 Zurich, Switzerland;2Ocean Spray Cranberries, Agriculture Research Group, Lakeville, Massachusetts 02349 USA; 3Institute ofAnimal Science, Swiss Federal Institute of Technology (ETH), 8092 Zurich, Switzerland

Accepted: August 12, 1997

Key words: Cydia pomonella, Lepidoptera, Tortricidae, flight distance, dispersal, flight mill, heritability, colonisa-tion

Abstract

Cydia pomonella L. (Lepidoptera: Tortricidae) is considered to be rather sedentary, but some individuals undertakeflights of several kilometres in the field. This paper investigates the genetic influence on this variability. Theflight capacity was measured in the laboratory by a flight mill and its heritability was estimated for two differentstrains. The laboratory strain was kept for more than 45 generations and the field strain from Embrach (northernSwitzerland) was recently collected in the field.

The multiple-trait-restricted-maximum-likelihood method was used for the estimation of genetic variances andcovariances. A mixed full-sib/half-sib design was applied for the field strain and a full-sib design for the laboratorystrain. The heritability of total distance was 0.57 for the field strain and 0.37 for the laboratory strain (both sexes).In addition, a heritability of 0.38 for total distance was estimated by parent-offspring regression for the laboratorystrain. All three values were significantly different from zero (P < 0:05) and show that there is a significant additivegenetic influence on flight capacity.

The genetic correlations between total distance and other flight traits (total duration, flight velocity, longestflight) were between 0.84 and 1.00 for both strains and suggest that these traits actually belong to a single one. Highgenetic correlations were also found between total distance and the morphological traits body weight and winglength for the field strain, whereas a negative correlation was found between total flight distance and body weightfor the laboratory strain. This difference between the two strains was interpreted as a possible trade-off betweenflight capacity and fecundity.

Introduction

The host plants of Cydia pomonella L. (Lepidoptera:Tortricidae) are various species of fruit trees (Barnes,1991). In northern Switzerland, the habitat of cod-ing moth is typically orchards and groups of appleor pear trees which are distributed in the landscape butoften found around villages. Such habitats may be con-sidered stable after the definition of Southwood (1977).The patchy distribution of suitable habitats means thatC. pomonella has a metapopulation structure in a broadsense, i.e. a set of conspecific populations linked bydispersal (Hastings & Harrison, 1994). Bues & Tou-

bon (1992), investigating enzyme polymorphism indifferent populations of C. pomonella in France andSwitzerland, observed considerable genetic similarityamong the populations, suggesting that there are sub-stantial flight movements between populations. Thismigratory flight behaviour is believed to function asthe linkage that keeps local populations together in ametapopulation (Hansson, 1991).

Mani & Wildbolz (1977) found that male codlingmoths may fly up to 11 km, and our work suggeststhat females have the same or even higher flight capa-city than males (Schumacher et al., 1997). Thus, it isprobable that there is significant moth movement even

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between patches as much as 10 km apart. Many factorsmay influence the percentage of moths which under-take such migratory, long-distance or inter-habitatflight, e.g., age and mated status (Schumacher et al.,1997). In our previous studies the variation of flightcapacity was found to be very large, even under homo-geneous environmental conditions in the laboratory(Schumacher et al., 1997). These results, along withthe significant difference in flight capacity between alaboratory strain and 4 field strains (unpublished data),suggest that there is a strong genetic effect on the vari-ability of flight capacity. It has been shown in otherinsects that flight capacity (as measured in tetheringexperiments) is a polygenic character and that its vari-ation has a significant additive genetic component (e.g.,Dingle, 1991).

The present study addresses the following twoquestions: first, is flight capacity measured by aflight mill potentially heritable? And second, what arethe genetic correlations amongst different flight para-meters investigated and between total flight distanceand morphological characters? A newly establishedfield strain was chosen for estimation of heritability.However, it is very difficult to pair field collected mothsunder laboratory conditions. Therefore, in a secondexperiment, which is considered as a replicate, a labor-atory strain was used for estimation of heritability des-pite its probably reduced genetic variability.

Materials and methods

Insect material and experimental design

Experiment A. Full- and half-sib families were estab-lished to estimate the heritability for the field collectedcodling moth strain from Embrach (northern Switzer-land). This design was chosen because the moths ori-ginating from the field did not mate after flight onthe flight mill and consequently the parent-offspringregression could not be used to estimate the heritabil-ity.

The insects were collected in August and Septem-ber 1994 near Embrach in the northern part of Switzer-land (450–500 m a.s.l.; 8�3601200–3700000 long. /47�3001600–2800 n. lat.). Moths originated from botha group of unmanaged high-stemmed apple trees anda nearby commercial orchard with dwarf apple trees.Corrugated paper protected with burlap fabric wasbound around the trunks of the trees to trap the fifthinstar larvae. The diapausing larvae were brought into

the laboratory and kept at constant darkness and 5 �C.Eight months later, the larvae were moved to 25 �C,65% r.h. and a photoperiod of L16:D8 for pupation(environmental conditions A). The emerged mothswere transferred to another climate chamber with alower temperature (20 �C) and a light regime withsimulated dusk and sunrise (environmental conditionsB), which was believed to be the most important factorfor the stimulation of mating and oviposition. Full light(c. 3500 lux) lasted for 16.5 h and the dark period (lessthan 0.5 lux) for 4.5 h. The increase and decrease inillumination were linear over a period of 1.5 h at duskand sunrise.

The moths were selected at random and releasedinto 1.5 l transparent cylinders (1 pair/cylinder) formating and oviposition. Both top and bottom of thecylinders were covered with nylon nets (1.5 mm mesh)to ensure sufficient ventilation. One immature appleper two oviposition cylinders was supplied for furtherstimulation of mating and oviposition. Under theseconditions 45% of the females from Embrach (n = 78)laid fertile eggs. The males of pairs with fertile eggswere moved into another oviposition cage and pairedwith a freshly emerged female. Only 17% of the males(n = 78) mated twice. This percentage was even lowerin another strain (3%,n = 49), which could not be usedfor the experiment because of the low number of fam-ilies available. This low proportion of males matingtwice seems also to be common under field conditionsas most of wild females caught in the field had onlyone spermatophore (Howell, 1988). Therefore, full-sib families were added to the half-sib families to getsufficient individuals for the estimation of heritabil-ity and the size of the families was not equal. Finally14 half-sib (7 sires) and 25 full-sib families (25 sires)with a total of 304 moths were tested for flight per-formance. The number of moths was different betweenfamilies. The larvae were reared on semi-artificial diet(Huber et al., 1972) under environmental conditionsA. Seventy-four % of the larvae went into diapauseand did not emerge within one month after cocooning.They were stored for 3 months at 4 �C and the emer-ging moths were tested 4 months later than the mothswithout diapause. The body weight and wing lengthof the moths were measured the day after emergence.Wing length was measured from the wing tip to thecentre of the thorax.

Experiment B. In the second experiment with a labor-atory strain the heritability was estimated using aparent-offspring design. The moths, which origin-

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ated from Wadenswil (northern Switzerland), had beenreared for over 45 generations in the laboratory. Theinbreeding coefficient, calculated after the methoddescribed in Falconer (1989), was estimated to liebetween 0.4 and 0.6 in relation to the original popula-tion. The larvae of the parents were reared on a semi-artificial medium (Huber et al., 1972) under environ-mental condition A. The matings of the parents weremade at random one day after emergence without con-sidering their flight capacity. Thirty larvae per familywere reared under conditions A, but at a lower tem-perature (20 �C). Twenty-four families with a total of157 sons and 145 daughters were considered for theanalysis. Body weight was measured three days afteremergence and before fight.

Fight mill technique

The same tethering and flight mill technique was usedas described in Schumacher et al. (1997). A pin wasaffixed on the back of the scale free thorax of the mothsusing a small amount of water-based glue. The pinwith the moths was fastened onto the balance arm (adrinking straw of 0.22 m length) of the flight mill. Apin pushed through the flight arm served as an axle,which was kept vertical by two magnets of each flightmill unit. Each revolution of each of the 30 flight millswas recorded by a computer. Out of this data, numberof flights, total duration, total distance, longest flightand flight velocity were calculated. All of these traitsexcept of the flight velocity needed to be transformedto satisfy the assumption of the analysis (Table 1).The distributions of the transformed data were visuallyassessed for normality. Whereas the duration of theobservations for the laboratory strain (Experiment B)was 2 h, the moths of the field strain (ExperimentA) were tested for 14 h. This resulted in a differentdistribution between the two experiments for the sametrait and hence a different transformation was appliedin the two experiments. The observations were madeunder environmental conditions B, but the light forexperiment B was kept constant between 2 to 5 lux.All moths of both experiments were tested 3 days afteremergence.

Estimation of heritability

The heritability was estimated with the programDFREML (Meyer, 1993). The parents in experimentB were not considered in this analysis, because theirrearing temperature was not the same as for the off-

spring. For this reason only full-sib families wereconsidered. This estimate is narrow sense heritab-ility that is possibly inflated by a portion of thenon-additive variance and maternal effects (Falcon-er, 1989). The program DFREML is designed formultiple-trait-restricted-maximum-likelihood estima-tion (Patterson & Thompson, 1971) of genetic vari-ances and covariances for the animal model (Meyer,1991). The animal model includes an equation foreach animal and a prerequisite for its application isthe availability of the additive genetic relationshipsmatrix. The use of the animal model is justified by thenumerous studies, where tethered flight performancehas been found to have a significant additive geneticvariance (e.g., Gu & Danthanarayana, 1992a). Sex wasincorporated as fixed factor in the model in both exper-iments. Diapause had to be included as an additionalfixed effect in the model of experiment A (field strain).

The heritability estimations were calculated inde-pendently for each trait, i.e. that only one trait at atime was considered. The sampling variances of theheritability estimates were calculated from a quadraticfunction fitted to the profile likelihood as described inMeyer & Hill (1992). The sampling variance (s2) is thesecond derivative of this function. Confidence intervalswere calculated as h2

+ z�=2S.Genetic correlations were calculated between the

trait total distance and all other traits which were con-sidered. These calculations had to be made pairwise,i.e., two traits were simultaneously processed.

Additionally, the heritability of total distance forthe laboratory strain (experiment B) was calculatedby parent-offspring regression, because this estima-tion represents the narrow-sense heritability. The cov-ariance between parent and offspring contains onlythe additive genetic component. However, it should benoted that a possible maternal effect would be includedin this covariance (Falconer, 1989). The phenotypic-al variance was not significantly different in the twosexes (variance ratio test; F = 0:006, n = 350,P = 0:94). Therefore, the regression on mid-parentvalues was used (Falconer, 1989). The mean flight dis-tance was significantly higher for the parents comparedto their offspring (Mann-Whitney U-test, n = 350,P � 0:001), as the rearing temperature has been 5 �Chigher for the parents. However, the variances werenot significantly different between parents and pro-geny (variance ratio test; F = 0:9, n = 24, P � 0:5)and the difference of the mean is believed to have noor only little influence on the slope of the regression.

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Table 1. Traits and their corresponding transformation to satisfy the assumptionfor the calculations of the heritability

Experiment Trait Transformation

A Total distance x0= SQRT(x) + SQRT(x+ 1)

Total duration x0= SQRT(x+ 1)

Longest flight (distance) x0= LN(x+ 1)

Longest flight (duration) x0= SQRT(x+ 1)

Number of flights x0= LOG10(x+ 1)

Velocity No transformation

Weight No transformation

Wing length No transformation

Weight/Wing length No transformation

B Total distance x0= LOG10(x)

Total duration x0= LOG10(x)

Longest flight (distance) x0= LOG10(x)

Longest flight (duration) x0= LOG10(x)

Number of flights x0= LOG10(x+ 1)

Velocity No transformation

Weight No transformation

Nevertheless, this does not rule out a possible temper-ature/flight interaction in heritability parameters.

Results

Heritabilities. The heritabilities of all flight traitsestimated by the animal model were significantly dif-ferent from zero (P < 0:05) with exception of that ofthe number of flights (Table 2). This was observed forboth the laboratory and the field strain. The highest her-itability (0.63) was found for total duration of the fieldstrain (Table 2). The heritabilities of total distance andtotal duration were higher for the field strain comparedto those for the laboratory strain, however, this differ-ence was not significant (Table 2).The strain differencebetween corresponding estimates was much smaller orabsent for the other flight traits and for body weight.The heritabilities of flight velocity of both strains werelow but still significantly different from zero, where-as the heritability of wing length was not significant.The estimate from the parent-offspring regression fortotal distance was 0.38 and almost identical to thatcalculated by the full-sib design (experiment B) andwas also significantly different from zero (Figure 1)(F = 4:322, P = 0:05, n = 24). Therefore, the invest-igation shows that the flight performance of C. pomon-ella has a significant additive genetic component.

Figure 1. Parent-offspring regression for total distance of codlingmoths from a laboratory strain (h2

= 0:38; F-Ratio = 4:322; P =

0:05, n = 24).

Genetic correlations. The genetic correlationsbetween total distance, total duration and longest flight(duration and distance) were 1.0 for both strains. Thegenetic correlations between total distance and flightvelocity was also very high (field strain: 0.8; laboratorystrain: 0.9) whereas the correlation between total dis-tance and number of flights was both lower and negative(field strain: 0.4; laboratory strain: 0.5). A high geneticcorrelation was found between wing length and totaldistance for the field strain (0.90). The genetic correl-

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Table 2. Heritability estimations (h2) and 95% confidence interval for flight and mor-phological traits of C. pomonella from a freshly established field strain (n = 304) and alaboratory strain (n = 302). The calculations are based on the animal model and a mixedfull-sib/half-sib design for the field strain and a full-sib design for the laboratory strain

Traits h2 and 95% confidence interval

Field strain Laboratory strain

Flight traits

Total duration 0.28 < 0.63 < 1,00 0.14 < 0.36 < 0.59

Total distance 0.30 < 0.57 < 0,86 0.15 < 0.37 < 0.59

Longest flight (duration) 0.11 < 0.40 < 0,70 0.15 < 0.37 < 0.59

Longest flight (distance) 0.10 < 0.41 < 0,74 0.15 < 0.38 < 0.60

Flight velocity 0.03 < 0.20 < 0,38 0.06 < 0.31 < 0.55

Number of flights �0:22 < 0.13 < 0,50 �0:19 < 0.05 < 0.29

Morphological trait

Body weight 0.02 < 0.21 < 0,41 0.09 < 0.32 < 0.54

Wing length �0:10 < 0.10 < 0,31

Weight/Wing length 0.03 < 0.22 < 0,41

ations between body weight and total distance werecontradictory between the two strains: the estimate forthe field strain was positive (0.44) while that for thelaboratory strain was negative (�0:32).

Discussion

Heritabilities. The heritability of flight capacity wasestimated for both a newly established field strain andfor a laboratory strain which was reared for over 45generations in the laboratory. For the field strain aheritability of 0.56 was estimated for total distance byusing the animal model with a design containing bothhalf- and full-sib families.

For the laboratory strain the heritability was lowerand almost identical if calculated by the parent-offspring regression (0.38) or by using the animalmodel for the full-sib families (0.37). This conform-ity between the two estimates is expected if additiveeffects are the major source of the genetic variation inthe trait (Falconer, 1989), and support the conclusionof Mousseau & Roff (1987). They found in their meta-analysis that there is no apparent bias introduced to thedata set by the method of heritability estimation. Ourresults argue that the variation in flight mill perform-ance in C. pomonella has an important additive geneticbasis. The heritabilities of tethered flight performancefor C. pomonella are comparable with those found for arange of other insects in different orders, e.g., Lygaeuskalmii (Hetereoptera; h2: 0.20 to 0.41; Caldwell &

Hegmann, 1969), Tribolium castaneum (Coleoptera;qualitative statement; Dıez & Lopez-Fanjul, 1979),Drosophila aldrichi (Diptera; h2: 0.21; Gu & Bark-er, 1995), Mythimna separata (Lepidoptera: Noctuid-ae; h2: 0.27; Han & Gatehouse, 1993) and Epiphyaspostvittana (Lepidoptera: Tortricidae; h2: 0.23 to 0.56;Gu & Danthanarayana, 1992a).

Genetic correlations. The genetic correlationsamongst the flight traits (total distance, total dura-tion, longest flight and flight velocity) were alwaysvery high (> 0:84) for both the laboratory strain andthe field strain. This close relationship is explained,first, by the functional dependence of flight velocityon total duration and total distance and, second, bypart-whole relationships among total distance, totalduration and longest flight. These findings are inform-ative in the design of future experiments as,genetically,the two parameter longest flight and total distance arealmost identical traits. Therefore, only one of thesetraits needs to be considered in further genetic analysis(e.g., selection experiment).

The genetic correlation between total distance andbody weight was positive for the field strain, but neg-ative for the laboratory strain. It remains open if thisdifference is significant or not, because the maximum-likelihood estimation of the model with two traits didnot allow the determination of an error term. However,an inconsistency of genetic correlation between totaldistance and body weight in the two strains couldhave two interesting explanations and is worth further

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investigation. First, it can be the effect of phenotypicplasticity on genetic correlations as the two strains werereared at two different temperatures. Such a phenotyp-ic plasticity was found in the tortricid moth Epiphyaspostvittana (Gu & Danthanarayana, 1992b). Second,this inconsistency of genetic correlations between thetwo strains may be also explained by the differenti-ation of the trait body weight. Higher body weight offemales may be produced by both a higher number ofeggs, e.g., higher fecundity, and a higher body mass,e.g., more flight muscle, larger wings or larger fatbody. This explanation is supported by the facts that thephenotypic correlation between fecundity and weightwas found to be positive for codling moth (Deseo,1971) and that the genetic correlation between flightdistance and wing length was very high in our study(0.90). Therefore, the negative correlation betweenflight distance and body weight in the laboratory strainmay be the result of selection for high fecundity andagainst flight capacity, whereas in the field strain high-er body weight points to higher flight capacity andlower fecundity. This is supported by the significantlylower mean fecundity of the field strain compared tothe laboratory strain (field: 36:8� 27:6 (mean � SE),n = 47; laboratory: 202:7 � 54:4, n = 90; Mann-Whitney U-test, P � 0:001). This indicates a pos-sible trade-off between flight and fecundity, as foundin many other studies (e.g., Gunn & Gatehouse, 1993;Gu & Danthanarayana, 1992b). This may be due to apleiotropic relationship between genes for flight capa-city and genes for fecundity.

Ecological significance. The distribution of flightdistance from short- to long-flying individuals willdepend on both the spatial (e.g., the degree of isol-ation and the size of the habitat, the number of new orvacant habitats) and temporal (mainly the permanencyof the habitat) characteristics of the habitat template(Southwood, 1977). The principal host of C. pomon-ella is apple, a fruit tree which reaches an age of over50 years. Therefore, the habitat of C. pomonella maybe considered as stable and the most successful eco-logical strategy for the moth would be to stay in thehabitat, e.g. it follows the ecological strategy ‘here andlater’ after the habitat suitability matrices of South-wood (1977). In this case, C. pomonella tends towardsa K-strategist (definition after MacArthur & Wilson,1967) and short-flying individuals would be favoured.Habitat destruction (death of the tree) may be con-sidered as rather rare. But the fruits are the resourceof codling moth and fruit production may fluctuate

between years because of biennial tendency in bearing,late frosts or severe attack by Anthonomus pomorum(Nagy, 1977). Therefore, the exclusive adherence toa short flight strategy would led to extinction in thecase of habitat destruction or the absence of fruits. Inthese cases, only migrants and their progeny wouldsurvive, provided that they find a new habitat. Hence,this temporal variation of the habitat preserves geneticvariation (Roff, 1994) and explains the large variationof flight distance in C. pomnella.

However, our understanding of the selection forcespromoting or acting against the long-flyers in a fieldpopulation is still very limited. To elucidate this point,further exploration of genetic covariances is necessaryto understand how the flight capacity will change inrelation to other traits (Roff & Mousseau, 1987).

Acknowledgements

We thank Cyrus Abivardi, Peter J. Edwards and HainanGu for valuable comments on the manuscript, ClaudeFornallaz for constructing the lighting, and Delia Sten-zel and Pia Rohr for technical assistance.

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