Anneli Hoikkala

Male courtship song frequency as an indicator of male genetic quality in an insect species, Drosophila montana

Most theoretical models on evolution of male secondary sexual characters and female preferences for these characters suggest that the male characters evolve in response to female preferences that may themselves evolve in response to direct or indirect benefits of choice. InDrosophila montana (a species of theD. virilis group), females use male song in their mate choice, preferring males that produce songs with short sound pulses and a high carrier frequency. We demonstrate here that the females get indirect benefits from their choice: in our data the frequency of the male song correlated with the survival rate of the males progeny from egg to adulthood (indirect benefit for the female), but not with the fecundity of his mating partner (no direct benefit for the female). Male wing centroid asymmetry did not correlate with male wing song characters, nor with female egg production nor the fitness of her progeny, suggesting that fluctuating asymmetry in male wings does not play a major role in sexual signalling. The fact that the male song gives the female information on the males condition/genetic quality inD. montana suggests that in this species the evolution of female preferences for male song characters could have evolved through condition–dependent viability selection presented in some ‘good genes’ models.

Male Mating Success and Survival in the Field with Respect to Size and Courtship Song Characters in Drosophila littoralis and D. montana (Diptera: Drosophilidae)

We investigated the importance of male song and morphological characters to the male mating success in a two-year field study in natural populations ofD. littoralis andD. montana. We compared the properties of mating flies with those of a random male sample taken at the same time and place. InD. littoralis the males size had no effect on his mating success, while inD. montana small males had a mating advantage in the field during the first study year. Females preferred males with short sound pulses in both species. We also examined the relationship between male morphological and song characters and viability by collecting male flies in late summer and comparing the means of male characters to those of overwintered flies the next spring. InD. littoralis male size had no effect on overwinter survival. InD. montana large flies survived better than small flies. In both species the shifts in song characters during the winter dormancy were opposite to those caused by sexual selection. Our results, accordingly, imply a possible balance between the forces of sexual and natural selection, which act in opposing directions on attractive male traits.

Courtship in Drosophila montana: the effects of male auditory signals on the behaviour of flies

Abstract In Drosophila montana (a species of the D. virilis group) the sounds produced by the courting male are a prerequisite for copulation. The mating behaviour of four experimental groups was recorded. Two groups consisted of single pairs of normal flies with successful and unsuccessful courtship, respectively. The third group consisted of single pairs of normal males and deaf females and the fourth group of single pairs of mute males and normal females. In successful courtships (i.e. those ending in copulation) touching and licking by the male led to female standing. Female standing led to male wing vibrating, male wing vibrating to female wing lifting, and female wing lifting to copulation. In unsuccessful courtships, the males did not vibrate their wings in response to female standing. In the groups lacking male auditory signals (deaf females or mute males) the females hummed their wings in response to male licking and wing vibrating. Although the males responded to wing humming by more licking and by producing more sounds, the courtships did not proceed to copulation. It is concluded that the willingness of the female to mate with a conspecific male depends on the detection of sound at the appropriate time in the courtship sequence as a response to female behaviour.

Laboratory and natural heritabilities of male courtship song characters in Drosophila montana and D. littoralis

We estimated heritabilities for several male courtship song characters in two Drosophila species using father-son regression under conditions where both fathers and sons had been raised in the laboratory. In D. montana the heritabilities of song characters were rather high (−0.23 to 0.80) and in most cases significant. In D. littoralis the heritabilities of song characters were generally lower (−0.33 to 0.18), and none of them was significantly larger than zero. We also estimated heritabilities regressing characters of wild-caught fathers with those of their laboratory reared sons, and used the method employed by Riska et al. to estimate the lower bound of heritabilities in nature. In D. montana most and in D. littoralis all of the across-environment heritabilities were non-significant (−0.15 to 0.43 and −0.04 to 0.15, respectively), and in some cases the across-environment heritabilities were significantly lower than the heritabilities measured under laboratory conditions. The low across-environment heritabilities appeared to be due to larger phenotypic variability of song characters in the field and in some cases also due to genotype-environment interactions.

Variation, but no covariance, in female preference functions and male song in a natural population of Drosophila montana

Studies of the variance and covariance between female mating preferences and sexually selected male traits in natural populations are rare. In D. montana, male courtship song is an important target of sexual selection. We analysed the variance in components of song and preferences among F1 families from a natural population. All song traits varied substantially, with among-family variance components ranging from 30 to 65%. The greatest variation was in carrier frequency, which is the most important predictor of mating success. This is compatible with the trait capturing mutational and other components of genetic variance in condition because of condition-dependent expression. There was also variation for some components of preference variation, with significant variation among sisters within families, and among families. Females varied in overall responsiveness, but not in the slope of the linear female preference function for male song carrier frequency. Such variation might be expected to generate assortative mating, with more choosy females mating with higher quality males, but there was no covariance across families between female responsiveness and male carrier frequency. Substantial variation in the level of responsiveness might allow low-quality males to achieve some mating success and counteract the build-up of a strong genetic covariance between preferences and traits.

Copulatory Courtship in Drosophila birchii and D. serrata, Species Recognition and Sexual Selection

Two endemic Australian Drosophila species, D. birchii and D. serrata, have a copulatory courtship, i.e., the males court the female mainly during copulation. In the present study we found the males of both species to mount their prospective mating partners selectively, exhibiting both sex and species recognition. The males began to sing after mounting the female, and they often exhibited also postcopulatory displays typical to copulatory courtship. D. birchii and D. serrata females discriminated against males which did not sing during mounting/copulation, which suggests that the females utilize cryptic female choice. Our findings raise the question of how widespread a phenomenon cryptic female choice is in Drosophila species.

Localization of genes affecting species differences in male courtship song between Drosophila virilis and D. littoralis

The males of six species of the Drosophila virilis group (including D. virilis) keep their wings extended while producing a train of sound pulses, where the pulses follow each other without any pause. The males of the remaining five species of the group produce only one sound pulse during each wing extension/vibration, which results in species-specific songs with long pauses (in D. littoralis about 300 ms) between successive sound pulses. Genetic analyses of the differences between the songs of D. virilis and D. littoralis showed that species-specific song traits are affected by genes on the X chromosome, and for the length of pause, also by genes on chromosomes 3 and 4. The X chromosomal genes having a major impact on pulse and pause length were tightly linked with white, apricot and notched marker genes located at the proximal third of the chromosome. A large inversion in D. littoralis, marked by notched, prevents more precise localization of these genes by classical crossing methods.

Copulatory courtship in Drosophila: behavior and songs of D. birchii and D. serrata.

D. birchii and D. serrata, two endemic Australian Drosophila species, have a copulatory courtship. The males of these species begin to court the female after mounting her and often go on with the courtship after the copulation is over. In the present paper we have described behavioral interactions between the male and the female and analyzed acoustic signals produced by the flies during courtship. Species differences were more pronounced in female than in male behavior. Variation within the species was obvious in the relative proportions of time the flies spent in different behaviors. Even though courtship took place nearly solely during copulation, some remains of precopulatory courtship were observed in both species. It is suggested that copulatory courtship exhibited by D. birchii and D. serrata flies is a derived rather than a primitive character.

Interactions of the Males and Females of Three Sympatric Drosophila virilis-Group Species, D. montana, D. littoralis, and D. lummei, (Diptera: Drosophilidae) in Intra- and Interspecific Courtships in the Wild and in the Laboratory

Four species of the Drosophila virilis group, D. montana, D. littoralis, D. lummei, and D. ezoana, occur sympatrically in several locations in northern Europe. Courtship interactions between the flies of the three first-mentioned species were observed at malt baits in Kemi, northern Finland, to find out how the flies of different species recognize conspecific individuals and how interspecific courtships differ from intraspecific ones in the wild. Intraspecific courtships (including females of different reproductive stages) and interspecific courtships were also videotaped and analyzed in laboratory. In the wild the males courted both conspecific and allospecific females, even though the species varied in how much the males were attracted to females of different species. Interspecific courtships usually broke off when the male touched the female or when the male and/or the female vibrated his/her wings, producing acoustic cues. In the laboratory males courted conspecific females irrespective of the reproductive stage of the female, even though the courtships directed toward immature and fertilized females usually included only orienting and touching (no licking and singing). D. littoralis, and very rarely D. montana and D. lummei, males courted also allospecific females. In the few interspecific courtships between these three species, where the male proceeded to singing, females responded to male singing by vibrating their wings. This ended the courtship. It is suggested that both the chemical cues affecting female attractivity and the acoustic signals of males and females, which are produced by wing vibration, function in maintaining sexual isolation between these three species.

QTL analysis of variation in male courtship song characters in Drosophila virilis

We have used a quantitative trait locus (QTL) mapping approach to study the genetic basis of differences between two Drosophila virilis strains representing extreme phenotypes in two song characters, the number of pulses in a pulse train (PN) and the length of a pulse train (PTL). Variation in these characters among 520 F2 males was studied by single-marker analysis and composite interval mapping (CIM) using a recombination linkage map constructed for 26 microsatellite markers. In single-marker analysis, two adjacent microsatellite markers on the third chromosome, msat19 and vir84 explained 13.8 and 12.4% of the variation in PN and 9.9 and 6.5% of the variation in PTL, respectively. CIM analysis revealed significant QTLs affecting PN, located on the X and the second, third and fourth chromosome of D. virilis, while variation in PTL was attributable to QTLs located only on the third chromosome.