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The role of male courtship behaviour in prezygotic isolation in NasoniaPeire Morais, Aitana

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5. Quantitative genetic analysis ofmale courtship in the parasitoid

wasp Nasonia vitripennis

Aitana Peire, Gerdien de Jong*, Ido Pen,Albert Kamping, Louis van de Zande and

Leo W. Beukeboom

* Evolutionary Population Biology, Utrecht University, Padualaan 8, 3584 CH, Utrecht, The Netherlands

05-Quantitative genetic 19/2/07 10:53 Página 83


Abstract

We analysed male courtship inheritance of the parasitoid waspNasonia vitripennis because divergence in courtship behaviour isconsidered an important pre-zygotic isolating mechanism. Previousstudies on interspecific hybrids between N. vitripennis and N.longicornis showed that male courtship behaviour has a complexgenetic basis with extensive epistatic and non-mendelian effects. Weinvestigated two main components of male courtship behaviour,headnod numbers and cycle duration. We used full-sib and nestedfull-sib half-sib designs, as well as phenotypic covariance betweenrelated males, to assess the amount of genetic variation as well aspresence and type of non-additive and epigenetic effects. We foundevidence of low genetic variation and no phenotypic correlationbetween both traits, suggesting independent genetic architectures.Maternal effects, and likely epistasis, were found to affect theexpression of headnod numbers. Inheritance of cycle duration wasaffected by parental male and female effects, which could beconsistent with genomic imprinting. These results confirm a complexinheritance of courtship behaviour within N. vitripennis. We discussthe significance of our results for the evolution of reproductiveisolation in the Nasonia complex.

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Introduction

Phenotypic differences between recently diverged speciesmay be informative about traits that have contributed to reproductiveisolation between species. Courtship behaviour is an obviouscandidate trait for playing a role in prezygotic isolation as it mightserve as a cue for species discrimination between closely relatedspecies (Coyne and Orr 1989). However, speciation is not the onlypossible cause for courtship divergence as sexual selection withinspecies (runaway selection, Maynard Smith 1991) or random drift canalso result in behavioural differences between species. Behaviouraltraits have often been found to have high levels of additive geneticvariance (Pomiankowski and Møller 1995; Merilä and Sheldon 1999;Boake et al. 2002) and to be modulated by non-additive geneticeffects, such as epistasis, dominance and/or environmental effects(Boake 1989; Ritchie and Kyriacou 1996; Meffert et al. 2002; Stirling etal. 2002; Hunt and Simmons 2002). Our research focuses on thegenetic architecture of courtship behaviour that may function as apossible prezygotic isolation mechanism in the Nasonia speciescomplex. Disentangling the underlying genetics of this behaviourmight help to understand the evolutionary processes that shaped it.

Nasonia are haplodiploid wasps, with haploid malesdeveloping from unfertilised eggs, and diploid females from fertilisedeggs. Behavioural genetic studies of haplodiploids are scarce andmainly restricted to the honey bee, Apis mellifera (Page and Erber2002). The pattern of inheritance in haplodiploids differs from diploidsand follows the same pattern as the X- chromosome in sexual systemswhere females have two X-chromosomes and males have one (Hartl1972; Grossman and Eisen 1989; Hedrick and Parker 1997). Parentalmales only contribute genes to males of the second generation (F2).Therefore, study of haplodiploids requires adjustments to quantitativegenetic parameter estimation (Hartl 1972, Crozier 1977, Lester andSelander 1979, Collins et al. 1984, Margolies and Cox 1993, Liu and

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The role of male courtship behaviour in prezygotic isolation in Nasonia...


Smith 2000). For male specific traits, haploid males need to becompared with males from two generations back (parental males) orwith the brothers of the F1 female (mother) they derived from.Moreover, the haploid male phenotype is not affected by dominanceinteractions which simplifies the detection of non-additive geneticeffects in the full sibs such as epistasis, imprinting or maternal effects.

The parasitoid wasp Nasonia has been the subject of studies ofcourtship behaviour over the past half century (Barrass 1960; van denAssem et al. 1980; van den Assem 1986; van den Assem and Werren1994; Beukeboom and van den Assem 2001, 2002). Starting from pureethological observations, studies have now advanced to dissect thegenetic architecture of behaviour using QTL mapping (Pietsch et al. inprep.). The genus Nasonia consists of three species, N. vitripennis, N.longicornis and N. giraulti each of which shows species-specificvariations to a general male courtship pattern (chapter 1). A malemounts on top of a female and starts performing headnodsaccompanied by the release of pheromones (van den Assem et al.1980). These movements are repeated along consecutive seriespunctuated by pauses. A cycle comprises the period between onset ofthe first headnod of two consecutive series. The average number ofheadnods in the different cycles and the duration of the cycles arespecies specific (van den Assem and Werren 1994; Beukeboom andvan den Assem 2001, 2002). Although studies of interspecific sexualisolation and female preference have shown varying degrees ofpremating isolation between Nasonia species (Bordenstein et al.2000; Velthuis et al. 2005), the causes of premating isolation are notfully understood and the role of male courtship behaviour in thespeciation process remains unclear.

Comparative courtship studies of hybrid males between N.longicornis and N. vitripennis showed a significant bias towards theparental male species’ behaviour in both reciprocal crosses (referredto as the “grandfather effect”, Beukeboom and van den Assem 2001).Although the experiment of Beukeboom and van den Assem (2001)seems to be only partially repeatable (chapters 3 and 6; Pietsch et al.

5. Quantitative genetic analysis of male courtship...

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in prep.) inheritance of male behaviour between different species orbehavioural lines within species often appears subject to non-additivegenetic effects (chapters 3 and 6). To rule out interactions betweensets of coadapted genes it is essential to study inheritance ofbehaviour within a single line.

In this study, we analysed genetic effects on phenotypicvariance of two main components of male courtship behaviour,headnod numbers and cycle durations, using recently collected N.vitripennis field lines. We used covariance between related males andfull-sib analysis in two populations and nested full-sib, half-sibanalysis (analogous to Lynch and Walsh 1998) in a third population.We discuss how knowledge about the genetic basis of male behaviourmight help to understand the genetic processes leading toreproductive isolation in Nasonia.

Material & Methods

Lines and culture conditionsNasonia wasps parasitise blowfly pupae (Protocalliphora andCalliphora). They are easily cultured in the laboratory having a gener-ation time of approximately two weeks at 25°C. The haplodiploid sexdetermining system makes it easy to obtain males, since virginfemales produce all male progenies and virgin females can easily becollected from hosts parasitised by mated females through opening flypupae before wasps emerge.

We used two recently collected N. vitripennis lines, one col-lected from a bait in Moscow (referred to as Mosc) and the other froma bird nest at the Zvenigorod Biological Station (referred to as Zven)60 km west of Moscow (Russia) in 2002. Microsatellite data showedthat the Mosc line was founded by at least two females (C. Berends,unpublished), but no molecular screening was performed on the

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Zven line that could have been founded by a single inseminatedfemale. Both lines were kept in diapause until 2003. We took them outof diapause and used them for experiments after two generations ofmaintenance in the lab. We chose these lines because they showedlarge differences in courtship behaviour. In addition, we established aline from a mixture of seven field lines collected in the Hoge VeluweNational Park (The Netherlands) in 2002. Each of these lines had beenkept in diapause separately since their collection. Our experimentsstarted after three generations of interbreeding them in the lab. Thisline is referred to as HogVel.

Courtship behaviourNasonia courtship behaviour is stereotypic and can easily beobserved and quantified (for details see van den Assem et al 1980, vanden Assem 1986; van den Assem and Werren 1994; chapter 1).Typically, Nasonia males mount the females and begin courtship, per-forming series of vigorous head movements, called headnods, punc-tuated by pauses. The first headnod in a series is accompanied by therelease of pheromones (van den Assem et al. 1980). A cycle is the timelapse between onset of the first headnod of two consecutive series.After a few series of headnods, a female may signal receptivity, andthe male backs up and copulates. If a female is already mated, shetypically does not become receptive again and the male eventuallydismounts. The number of headnods in the first four series werescored, as well as the cycle time. These are the main components ofthe courtship display and differ quantitatively between the species.

Observations were performed under lab conditions at 25º witha stereo binocular microscope. Individual males were placed in 60mm glass tubes, diameter 10mm, closed off with a plug of cottonwool, and mated test females were then introduced. Cycle durationswere measured with a stopwatch. All males were inexperienced andone-day old, since male age and previous experience may have aneffect on the courtship performance (Beukeboom and van den Assem2001).


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Breeding designA full sib analysis was performed with the two Russian lines todetermine the components of phenotypic variance of male courtshipbehaviour (see below “Quantitative Genetic Analysis”). The breedingdesign is shown in figure 1. For each line 50 parental couples (P) wereestablished by placing a single male with a single female. Biparentallyproduced F1 females were set up as virgins and produced the F2haploid males. Two F2 males derived from one F1 female per parentalcouple were analysed. Brothers derived from the same F1 female arefull sibs. To calculate covariances between related males we scoredthree F1 males that were sons of the same female, per parental female.For the same purpose, we scored the behaviour of the parental males.

A nested full-sib, half-sib analysis was performed with theHogVel line by mating 50 males each to two randomly selectedfemales (Figure 2). Hosts were replaced every other day for four timesto have supply of males for several consecutive observation days. Thedifference with the full sib analysis is that F2 half sib males (HS) sharethe parental male but not the parental (and F1) female, hence F2males are half sibs in addition to full sibs (FS). Comparison betweenhalf sibs and full sibs permits discrimination between epistasis oreffects of genes derived from parental females (shared by full sibs)and effects due to genes derived from parental males (shared by halfsibs). We reared F1 females as virgin, hosted one per family andscored three F2 males per F1 female. To calculate covariance betweenrelatives we scored behaviour of parental males and of two F1 malesper cross.

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Figure 1. Full sib design for haplodiploids.In the grandparental generation a male is mated to an unrelatedfemale. The F1 generation consists of males derived from themother only and diploid females from both the parental father andmother. F2 haploid males are sons of the F1 mothers. Sons of thesame mother (within a box) are full sibs, and there are two

generations of full sibs: F1 and F2.


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Figure 2. Nested half-sib full-sib design for haplodiploids.

Parental males are mated to two unrelated females. The F1generation consists of males derived from the mother only anddiploid females from each of the mothers and the shared father. F2haploid males are sons of the F1 mothers. Sons of the same mother(within a box) are full sibs, and there are two generations of fullsibs: F1 and F2. F2 sons of both mothers share the same

grandfather are half sibs.

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Quantitative genetic analysisTo avoid comparison between non-independent variables weperformed a correlation analysis with the different elements ofbehaviour. Headnod numbers of the first four series were highlycorrelated among each other as were cycle durations of the first threeseries (see Results). Therefore, we calculated one first principalcomponent (Jolliffe 2002) of the first four series of headnod numbersand one of the duration of the three first cycles, which yielded onecomposite measure of headnod numbers and one of cycle duration.

The phenotypic variance (VP) can be partitioned as

VP = VE + VG

where for haploid males

VG = VA + VI + pf

VE is the variance due to environmental effects, VG is the variance dueto genetic effects, VA is the additive genetic variance, VI is the variancedue to epistasis and pf denotes effects from the parental female.Effects from the parental female generally refer to cytoplasmic factorsand they will be roughly similar to effects from the F1 females,although differences could arise from cytoplasmic factors that dependon the nuclear genes (different between P and F1 females). Todetermine different contributions of parental male and femalegenotype in the F2 male phenotype we divided VA into the additivegenetic variance of the genes derived from the parental male (VApm),the genes derived from the parental female (VApf) and twice thecovariance between the two (CovApm, Apf):

VA = VApm + VApf + 2 CovApm,Apf

Full sib males are the offspring of the same parents indiploids and the F2 males derived from the same parental couple inhaplodiploids. Full sibs share additive effects of the genes in the totalphenotypic variance, but also epistatic and maternal effects from theparental female (Falconer and Mackay 1996; Tables 1 and 2).


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Half sib males share only one of the parents in diploids. Inour set up F2 half sibs shared the parental male and resemblanceamong them was predicted to be due to additive effects of the genes,epistasis and, if present, effects from the parental male, since all theadditive genetic variance calculated from resemblance among halfsibs is due to genes derived from the parental males (Table 2).

We estimated the components of variance within eachexperiment with the method of restricted maximum likelihood (REML)using Statistica, which yields asymptotic (for large sample size) standarderrors. The effects of sires in the full sib analysis and sires and damswithin sires in the nested analysis were considered as random.

Phenotypic covariance between relatives allows to identifynon-additive genetic effects when compared to the covariances fromanalysis of sibs. In haplodiploids two generations are necessary toobtain males related to the parental males (Figs. 1 and 2). Wecalculated covariances between F2 males and both parental and F1males. In addition to non-additive genetic contributions to phenotypicvariance, it permitted calculation of relative contribution of parentalfemale and male to the additive genetic variance in full sibs.

Table 1. [In the next page]Full sib analysis, phenotypic covariance between relatives andpartition of variance of the first principal component of twocourtship components in the Russian lines (Mosc and Zven).Standard errors (SE) of the variance components are asymptotic (forlarge samples). Components of variance from restricted maximumlikelihood (REML): Sires are males of different families; Sibs withinsires are full brothers (derived from the same parental male andfemale). Covariances: Pm:, phenotypic covariance betweenparental and F1 males, F1: phenotypic covariance between F1 andF2 males. VG: genetic variance; VA: additive genetic variance; VI:variance due to epistasis; gm: grandmaternal effects; VAPm, VAPf:

additive genetic variance of genes derived from the parental malerespectively female in F2 males and CovAPm,APf: covariance

between the two; *P<0.05; **P<0.01; ***P<0.001; n.s.: P>0.05.

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Contributions of the different factors to phenotypic variance canbe calculated from the phenotypic variance or covariance betweenrelatives and their coefficient of relatedness r (Lynch and Walsh 1998p.145). In haplodiploids the coefficient of relatedness between haploidmales is 1/4 for half sibs, 1/2 for full sibs, 1/2 between parental and F2males and 1/4 between F1 and F2 males (Grossman and Eisen 1989).

Under our controlled conditions, we assume that VE is thesame in all treatments, and therefore it does not affect the differencesbetween estimates. If the genetic variance is determined only byadditive effects of genes, then the variance component for full sibsand the covariance between parental and F2 males must equal, sincethey both represent 1/4 of VA (Tables 1 and 2). Under purely additivegenetic effects (VA), twice the covariance for F2 and F1 males wouldequal as well half of the VA. Finally, the variance calculated for halfsibs, where available, would equal the covariance between F1 and F2males. Thus, under additive genetic effects alone,

VFS = CovP,F2 = 2 CovF1,F2 = 2 VHS, which corresponds to:

1/2 VA = 1/2 VA = 2 1/4 VA = 2 1/4 VA

where FS is full sibs, P is parental males, F1 and F2 are males from theF1 respectively F2 generation, and HS is half sibs.

With epistasis (VI) twice the covariance between F1 and F2males and the variance of half sibs would be lower than the variancefor full sibs and the covariance between parental and F2 males:

VFS = CovP,F2 > 2 CovF1,F2 = 2 VHS, which corresponds to:

(1/2 VA + 1/4 VI) = (1/2 VA + 1/4 VI) > 2 (1/4 VA + 1/16 VI) = 2 (1/4 VA + 1/16 VI)

With no epistasis and under effects of the parental female (pf)twice the variance of half sibs would equal the covariance betweenparental and F2 males and would be lower than the variance of fullsibs. The variance of full sibs would also be lower than twice thecovariance of F1 and F2 males:

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2 VHS = CovP,F2 < VFS < 2 CovF1,F2, which corresponds to:

2 1/4 VA = 1/2 VA < (1/2 VA + pf) < 2 (1/4VA + pf)

If genes derived from the parental male (Pm) or female (Pf) aredifferently expressed, the contribution to additive genetic variancefrom male genes (VAPm) would be different from the contributionfrom female genes (VAPf) and their covariance would also differ(CovAPm, APf). Under additivity the contributions are equal and allthree values are equal as well. Thus:

VAPm > VAPf =/ CovAPm, APf under preferential expression of malegenes

and

VAPm < VAPf =/ CovAPm, APf under preferential expression of female

genes.

Differences between VAPm and VAPf would show up asdifferences between CovP,F2, that includes 1/4 VAPm and 2CovF1,F2 thatincludes 1/4 VApf (specifically, 2 (1/8 VApf)). It should be noted that wecannot distinguish the exact mechanism of preferential expression(for example, silencing of genes or cytoplasmic effects) causingbiased expression with the current experimental design. We did notestimate significance of the comparisons since our limited samplesizes yielded too high standard errors and high chances of type IIerrors (false negatives).

Table 2. Nested sib analysis, phenotypic covariance between relatives andpartition of variance of the first principal component of twocourtship components in the Hoge Veluwe (HogVel) line. Standarderrors (SE) of the variance components are asymptotic (for largesamples). Components of variance from restricted maximumlikelihood (REML): Sires are males of different families; Dams withinsires are males derived from the same parental male but differentparental female; Sibs within sires are males derived from the sameparental male and female. Covariances: P and F1: phenotypic


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covariance between parental and F2 respectively F1 males. VG:genetic variance; VA: additive genetic variance; VI: variance due toepistasis; gm: grandmaternal effects; VAPm, VAPf : additive geneticvariance of genes derived from the parental male respectivelyfemale in F2 males and CovAPm,APf: covariance between the two;*P<0.05; **P<0.01; ***P<0.001; n.s.: P>0.05.

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ResultsCourtship behaviourMales from the two Russian and the Hoge Veluwe lines showedstereotypical courtship behaviour, but with significant differencesbetween them. The average number of headnods in the first seriesranged from 4.70 (Zven) to 6.22 (Mosc), with a decrease of 1-1.5 nodsin the second series followed by an increase in the subsequent series,as is typical for N. vitripennis (Table 3). Cycle durations ranged from7.44 (HogVel) to 8.46 sec (Mosc) and remained relatively constantbetween series.

Consistent and significant correlations were found between thenumber of headnods in subsequent series and between the cycledurations (Pearson correlation coefficients for the headnods series rangefrom 0.12 to 0.68, with P<0.001, except the 1st series that is only signi-ficantly correlated with the 3rd series, with P<0.01; for cycle durations therange is from 0.75 to 0.60 with P<0.001; Table 4, data shown for Moscline only), while headnod numbers are not correlated to cycledurations, indicating that both traits are phenotypically independent.

Quantitative genetic analysisFull sibs. We found a significant component of sires (brothers

derived from the same F1 female) in the Zven line for headnodnumbers, where it represents 34% of the total phenotypic varianceand for cycle durations, where it represents 52% of the total variance(Table 1), indicating the presence of genetic variability in this line. Inthe Mosc line effects of sires are not significant, indicating low (ornone) genetic variation.

Half sibs. Neither sires nor dams effects are significant inheadnod numbers in the HogVel line, indicating low or no geneticvariation (Table 2). In cycle duration effects of dams are significantand account for 25% of the total variance, while sires are marginallysignificant (p=0.08) and account for 18% of the total variance (Table2). This points to the presence of variation for this trait and a weakeffect of genes derived from the parental male.


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Table 4. Pearson correlations between male courtship components in the Mosc

line.*P<0.05; **P<0.01; ***P<0.001; n.s.: P>0.05.

Phenotypic covariance. We only found a significantcovariance between related males in cycle durations between P and F1males of the Zven line, but not in the Mosc and HogVel line, nor inheadnod numbers in any of the three lines. Despite the non-significantresults (see Material and Methods), comparison between the differentestimates of variance and covariance was useful to estimate thecomponents of phenotypic variance. In the HogVel line we comparedthe values obtained from partitioning the additive genetic variance(VA) into VAPf and VAPm when we only used sibs, to the values whenwe used full sibs and covariances between F2 males and P or F1 males.Interestingly, we found that if half sibs were not taken into accountVAPm was overestimated, whereas VAPf and the covariance betweenthe two (CovAPm,APf) were underestimated by the same amount (VAPfand CovAPm,APf underestimated by 0.453 in headnod numbers and by


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0.604 in cycle duration). The estimation bias was likely a consequenceof overestimation of the covariance between P and F2 males, sincesubstracting half the difference corrected the bias, while adding halfthe difference to the covariance between F1 and F2 males onlychanged the direction of the bias towards higher VAPf and CovAPm,Pfand lower VAPm. We therefore took into account a possibleoverestimation of VAPm in the discussion of the results.

In headnod numbers we found evidence of parental femaleeffects in the HogVel and Zven lines. In both lines the only conditionnot satisfied under effects of the parental female was that twice thecovariance between F1 and F2 males (CovF1,F2) was roughly equalinstead of larger than the variance for full sibs (VFS; Tables 1 and 2). Apossible reason for this is that F1 and F2 males only share half theeffects of the parental female (pf), perhaps because genes of the F1females also play a role in increasing the variance of full sibs. In theMosc line VFS and the covariance between P and F2 males (CovP,F2)had similar values, while 2CovF1,F2 was lower (Table 1). Takentogether, results for the Mosc line fit a model with additive andepistatic effects on headnod numbers. However, if CovP,F2 wasoverestimated it would be lower than VFS and perhaps also lower than2CovF1,F2, which would fit a model with effects of parental females.But in that case twice CovF1,F2 should be larger than VFS, while it issmaller (.2 CovF1,F2 = 0.04; VFS = 0.45). Either there were strong effectsof F1 females inflating VFS, or headnod numbers were under additiveand epistatic effects in the Mosc line.

In cycle durations we found no pattern in the variancescompatible with simple additive, epistasis or effects of parentalfemales in the HogVel line. In the Mosc line the only condition notsatisfied for effects of parental females was that VFS was lower thanCovP,F2. If this covariance was overestimated in the Mosc line (seeabove “phenotypic covariance”) our results would be consistent witheffects of parental females. In the Zven line a large overestimation ofCovF1,F2 and strong effects of F1 females inflating VFS could make ourresults compatible with effects of parental females, but partition of the

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VA into VAPf and VAPm shows an effect of genes of parental males 2.6times higher than genes of parental females and a negative covariancebetween the two (VAPf = 1.267; VAPm = 3.249; CovAPm,Pf = -3.522).Similar values are found from the analysis of sibs in the HogVel linewhere VAPm is 2.5 times higher than VAPf and CovAPm,APf is almost zero(VAPf = 0.672; VAPm = 1.705; CovAPm,Pf = 0.051). These results suggestan effect of parental males in cycle duration of the HogVel line andperhaps, although less evidently, of the Zven line.

In summary, we found variation for effects of parental females,additive and epistatic effects modulating headnod numbers, and foreffects of parental males or parental females influencing theexpression of cycle durations. Thus, inheritance of male behaviourwithin a line is also affected by non-additive effects, consistent withthe results found between behavioural lines within a species andbetween species..

Discussion

Three methods, full-sib and nested full-sib half-sib designs as well asphenotypic covariance between related males were used to analysethe inheritance of two characters of male courtship behaviour,headnod numbers and cycle duration, in two Russian and a mix ofDutch lines of the parasitic wasp Nasonia vitripennis. We found nophenotypic correlation between the two characters, which suggestsindependent genetic architectures, allowing each trait to responddifferently to evolutionary forces. In addition, we compared varianceand covariance components in male behaviour to estimate additivegenetic and non-additive effects. One of the recently collectedRussian lines (Zven) founded by at least one inseminated female, wasthe only one to show significant genetic variation in both traits, whilethe mix of Dutch lines (HogVel) showed significant variation in cycle


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duration but not in headnod numbers. We found evidence for non-additivity in both traits but effects were variable for the same trait indifferent lines and between the traits within lines. While we foundindications of parental and F1 female effects and possibly epistasis inthe expression of headnod numbers, inheritance of cycle durationappeared affected by either parental males or females, perhapsreflecting genomic imprinting. Maternal effects (effects of F1 females)are generally predicted in haplodiploids, and supposed to be at thebasis of eusociality in Hymenoptera (Wade 2001), while the evolutionof genomic imprinting is expected for traits under sex specificselection (Day and Bonduriansky 2004).

Genetic variation and non-additive effectsDespite the low values of additive genetic variance, genetic

variation can still exist but be concealed by other factors such asepistasis or environmental effects (Hedrick 1988; Ritchie and Kyriacou1996; Merilä and Sheldon 1999). Epistasis might play a role incanalising phenotypic expression of behavioural traits understabilizing selection, making the phenotype less dependent of theunderlying genetic variation (Pomiankowski and Møller 1995; Meffertet al. 2000; Hermisson et al. 2003). We found some evidence ofepistasis affecting headnod numbers in one of the lines (Mosc).Furthermore, in a recent QTL analysis of male courtship behaviour inNasonia hybrids many epistatic interactions were found to affect theexpression of these traits (Pietsch et al. submitted). On the other hand,in the absence of additive genetic variance, maternal effects mightcreate adaptive phenotypic variability in behavioural traits (e.g.Forstmeier et al. 2004). We found evidence of parental female effectsin headnod numbers in two of the three analysed lines, Zven andHogVel. Parental males seemed to differentially affect expression ofcycle durations in the HogVel line and, less clearly, in the Zven line.The fact that non-additive effects are not consistent in the three linessuggests the existence of variation for non-additive effects on malebehaviour. In the HogVel line a strong indication of male parental

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effects came from the comparison of the proportion of the totalphenotypic variance explained by the half sibs. Half sibs represented18% (p = 0.08) while full sibs represented 25% of the variance(p<0.01). In addition, both in the HogVel line and in the Zven linecontribution of parental male genes to the additive genetic variancewas estimated to be 2.5 times larger than that of parental femalegenes. Perhaps parental male and female effects have the sameunderlying mechanism and it would be interesting to determine theforces that favour the expression of genes of one parent over thegenes of the other.

Differential expression of genes is comparable to dominanceeffects, as it happens under genomic imprinting, where genes of onesex are differentially silenced (Anderson and Spencer 1999).Dominance is expected to evolve in traits under selection to favourexpression of advantageous alleles (Boake et al. 2002). Haploidmales do not have dominance interactions, but fitness of individualswith a combination of favourable and deleterious alleles would beincreased if favourable alleles were preferentially expressed anddisadvantageous alleles were silenced (Day and Bonduriansky2004). However, our data do not warrant that imprinting affects malebehaviour in Nasonia. Perhaps complex epistatic interactions canaccount for favourable genes preferentially expressed (chapter 3) andthe particular mechanisms need to be elucidated in futureexperiments. In general, we have found an extensive role of non-additive genetic effects underlying male courtship behaviour withindifferent lines of N. vitripennis, consistent with previous studies onhybrids between species and of line crosses within a species(Beukeboom and van den Assem 2001, 2002; Pietsch et al. submitted;chapters 3 and 6).

Selection and speciation.In North America N. vitripennis populations are sympatric with eitherof the sibling species N. longicornis or N. giraulti. Species arereproductively isolated by Wolbachia-induced cytoplasmic


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incompatibility (Werren 1997; chapter 1) setting the conditions forevolution of prezygotic isolation to avoid the cost of hybrid matings(Bordenstein and Werren 1998). One important source of prezygoticisolation between closely related species is divergence of malecourtship behaviour and associated female preference (reinforcementof prezygotic isolation; e.g. Noor 1999). However, male behaviour mayalso be an indicator of male quality in intraspecific sexual selection(Maynard Smith 1991). The absence of sympatric sibling species in theEuropean populations suggests that the latter type of selection wouldbe more important in the populations analysed in our present study.The complex genetic architecture of courtship behaviour makes itdifficult to resolve how selection may act. Moreover, to assess theimportance of non-additive effects in the speciation process it isnecessary to determine the role of male behaviour in sympatricpopulations of the three Nasonia species.

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