Behavioral genetics of Drosophila ananassae

Drosophila ananassae has a unique status among Drosophila species because of certain peculiarities in its genetic behavior. The most unusual feature of this species is its relatively high frequency of spontaneous male recombination. The results of studies on non-sexual behavior, such as phototactic responses, eclosion rhythm, and preferences for oviposition and pupation sites, lead us to suggest that this behavior is under polygenic control, with a substantial amount of additive genetic variation. Sexual isolation has been reported in D. ananassae with the degree of such isolation being stronger in isofemale lines than in natural populations. The significant variations seen in the mating propensity of several isofemale strains, inversion karyotypes and wild type strains, the diminishing effects of certain mutations on the sexual activity of males, and the positive responses to selection for high and low mating propensity point to a genetic control of sexual behavior in D. ananassae. Males contribute more to variation and thus are more subject to intrasexual selection than females. There is a positive correlation between sternopleural bristle number, mating propensity and fertility in D. ananassae. This correlation between morphometric traits and mating success suggests that larger flies are more successful in mating than smaller ones. There is also evidence for adaptive plasticity and a trade-off between longevity and productivity in D. ananassae. Rare, specific courtship song parameters that provide males with a mating advantage have also been reported in different geographic strains of D. ananassae. The remating behavior of males and females, sperm displacement, and the bi-directional selection for female remating speed indicate that post-mating behavior in this species may also be under genetic control. The occurrence of size assortative mating further indicates that there is size-dependent sexual selection in D. ananassae.     

Variation in mating propensity and fertility in isofemale strains of Drosophila ananassae

Mating propensity and fertility were studied in five laboratory strains of Drosophila ananassae which were established from single females collected from different geographical localities. The results show statistically significant variation among different isofemale lines with respect to mating propensity and fertility. The strains showing greater sexual activity produce more progeny. Thus, there is a positive correlation between mating activity and fertility in D. ananassae. The comparison of mating frequencies of strains and their hybrids reveals the existence of heterosis and reciprocal effects. The data suggest that the males are more subject to intrasexual selection.     

Long-term selection for a quantitative character in large replicate populations of Drosophila melanogaster

Summary Six replicate lines of Drosophila melanogaster, which had been selected for increased abdominal bristle number for more than 85 generations, were assayed by hierarchical analysis of variance and offspring on parent regression immediately after selection ceased, and by single-generation realised heritability after more than 25 generations of subsequent relaxed selection.Half-sib estimates of heritability in 5 lines were as high as in the base population and much higher than observed genetic gains would suggest, excluding lack of sufficient additive genetic variance as a cause of ineffective selection in these lines. Also, there was considerable diversity among the six lines in composition of phenotypic variability: in addition to differences in the additive genetic component, one or more of the components due to dominance, epistasis, sex-linkage or genotype-environment interaction appeared to be important in different lines.Even after relaxed selection, single-generation realised heritabilities in four lines were as high as in the base population. As a large proportion of total genetic gain must have been made by fixation of favourable alleles, the compensatory increase of genetic variability has been sought in a genetic model involving genes at low initial frequencies, enhancement of gene effects during selection and/or new mutations.     

Bottleneck Effects on Genetic Variance for Courtship Repertoire

Bottleneck effects on evolutionary potential in mating behavior were addressed through assays of additive genetic variances and resulting phenotypic responses to drift in the courtship repertoires of six two-pair founder-flush lines and two control populations of the housefly. A simulation addressed the complication that an estimate of the genetic variance for a courtship trait (e.g., male performance vigor or the female requirement for copulation) must involve assays against the background behavior of the mating partners. The additive ``environmental' effect of the mating partner's phenotype simply dilutes the net parent-offspring covariance for a trait. However, if there is an interaction with this ``environmental' component, negative parent-offspring covariances can result under conditions of high incompatibility between the population's distributions for male performance and female choice requirements, despite high levels of genetic variance. All six bottlenecked lines exhibited significant differentiation from the controls in at least one measure of the parent-offspring covariance for male performance or female choice (estimated by 50 parent-son and 50 parent-daughter covariances for 10 courtship traits per line) which translated to significant phenotypic drift. However, the average effect across traits or across lines did not yield a significant net increase in genetic variance due to bottlenecks. Concerted phenotypic differentiation due to the founder-flush event provided indirect evidence of directional dominance in a subset of traits. Furthermore, indirect evidence of genotype-environment interactions (potentially producing genotype-genotype effects) was found in the negative parent-offspring covariances predicted by the male-female interaction simulation and by the association of the magnitude of phenotypic drift with the absolute value of the parent-offspring covariance. Hence, nonadditive genetic effects on mating behavior may be important in structuring genetic variance for courtship, although most of the increases in genetic variance would be expected to reflect inbreeding depression with relatively rare situations representing the facilitation of speciation by bottlenecks.     

Androgen influence on mating behavior in selected lines of Japanese quail

Bidirectional selection for high and low mating behavior has resulted in lines of Japanese quail that differ significantly in mating frequency. To evaluate the effects of this selection on the endocrine aspects of mating behavior, exogenous testosterone cypionate (TC) was administered to caponized and intact males from selected and control lines. Dosages of TC, administered as a single injection, were 0, 5.0, and 10.0 mg for the caponized and 1.25, 2.5, and 5.0 mg for the intact males. Mating performance was measured by testing each male individually with a series of female tester-flocks for eight 8-min periods.Capons mated within 3 to 4 days postinjection, with the period of peak activity occurring between the eighth and twelfth days. Hypertrophy of the cloacal gland followed a similar pattern. At no TC level was the mating frequency of caponized males from the low mating line equal to that of males from the high mating line. Furthermore, exogenous TC at these dosages failed to stimulate capons from the high and low mating lines to mate as frequently as the intact males of their respective lines. Exogenous TC had a depressing effect upon the mating frequency of intact males from the high mating and control lines but had no influence on those from the low mating line.     

No genetic correlation between the sexes in mating frequency in the bean beetle, Callosobruchus chinensis

Female multiple mating, which is common in animals, may have evolved not in response to fitness advantages to females but as a genetic corollary to selection on males to mate frequently. This nonadaptive hypothesis assumes a genetic correlation between females and males in mating frequency, which has received a few empirical investigations. We tested this hypothesis by observing the correlated response in male mating frequency in the adzuki bean beetle, Callosobruchus chinensis to artificial selection on female propensity to remate. Compared to control females, females from lines selected for increased or decreased female propensity to remate had, respectively, higher or lower mating frequency measured by the number of mating within a given period. This indicates that female receptivity to remating is genetically correlated with female mating frequency, and thus the artificial selection for female propensity to remate influenced female mating frequency. In contrast, males from the selected lines that diverged in female mating frequency did not vary significantly in their mating frequency. These results indicate that there is no genetic correlation between the sexes in mating frequency in C. chinensis. This study shows that the reason why females in C. chinensis remate despite suffering fitness costs cannot be explained by indirect selection resulting from selection on males to mate multiple times.     

The Costs of Reproductive Success in Male Rhesus Macaques (Macaca mulatta) on Cayo Santiago

Sexual selection acts to increase the success of males possessing advantageous traits in competition over females. In primates, interspecific variability in social and mating systems creates highly variable selective pressures on males, changing the relative strength of both intra- and intersexual selection, and the relative degree of direct vs. indirect male–male competition. Rhesus macaques are an interesting species for studying intrasexual selection and male–male competition, because they exhibit relatively low (for Papionini) body and canine size dimorphism, and exhibit large testes, suggesting reduced direct competition and strong indirect competition. We have undertaken several studies of male rhesus macaques on Cayo Santiago, from analyses of long-term life-history data to shorter term projects that combined noninvasive measures of physiological markers such as concentrations of urinary C-peptide of insulin and androgen and glucocorticoid (GC) concentrations, with measures of behavior and of sexually selected signals (male red facial coloration). We here review these studies, combining data from short-term studies with long-term mortality data to present an integrated picture of both the short- and long-term gross costs of male mating competition. We find that males exhibit many signs of the costs of indirect competition, such as energetic consequences of reduced feeding and high copulation rates. During periods of more direct contest, such as during dominance instability, males are also characterized by high androgen and GC concentrations among high-ranking individuals. Consistent with relatively weak direct male–male competition, male red skin coloration appears to be more related to female choice (intersexual selection) than the signaling of dominance status (intrasexual selection). Forty-five years of life-history data show that male mortality is higher during the mating than the birth season, a pattern we hypothesize to be linked to the costs associated with mating activity. We finish by discussing unresolved issues, such as the costs of sperm competition and the data that are needed to address them.     

Interpopulation variation in female remating is attributable to female and male effects in <Emphasis Type="Italic">Callosobruchus chinensis</Emphasis>

The evolution of female multiple mating is best understood by consideration of male and female reproductive perspectives. Females should usually be selected to remate at their optimum frequencies whereas males should be selected to manipulate female remating to their advantage. Female remating behavior may therefore be changed by variation of male and female traits. In this study, our objective was to separate the effects of female and male strains on female remating for the adzuki bean beetle, Callosobruchus chinensis, for which there is interstrain variation in female remating frequency. We found that interstrain variation in female remating is primarily attributable to female traits, suggesting genetic variation in female receptivity to remating in C. chinensis. Some interstrain variation in female remating propensity was attributable to an interaction between female and male strains, however, with the males of some strains being good at inducing nonreceptivity in females from one high-remating strain whereas others were good at inducing copulation in nonvirgin females from the high-remating strain. There is, therefore, interstrain variation in male ability to deter females from remating and in male ability to mate successfully with nonvirgin females. These results suggest that mating traits have evolved along different trajectories in different strains of C. chinensis.     

Reversed selection responses in small populations of the housefly (Musca domestica L.)

We compared the efficacy of artificial and natural selection processes in purging the genetic load of perpetually small populations. We subjected replicate lines of the housefly (Musca domestica L.), recently derived from the wild, to artificial selection for increased mating propensity (i.e., the proportion of male–female pairs initiating copulation within 30 min) in efforts to cull out the inbreeding depression effects of long-term small population size (as determined by a selection protocol for increased assortative mating). We also maintained parallel non-selection lines for assessing the spontaneous purge of genetic load due to inbreeding alone. We thus evaluated the fitness of artificially and ‘naturally’ purging populations held at census sizes of 40 individuals over the course of 18 generations. We found that the artificially selected lines had significant increases in mating propensity (up to 46% higher from the beginning of the protocol) followed by reversed selection responses back to the initial levels, resulting in non-significant heritabilities. Nevertheless, the ‘naturally’ selected lines had significantly lower fitness overall (a 28% reduction from the beginning of the protocol), although lower effective population sizes could have contributed to this effect. We conclude that artificial selection bolstered fitness, but only in the short-term, because the inadvertent fixation of extant genetic load later resulted in pleiotropic fitness declines. Still, the short-term advantage of the selection protocol likely contributed to the success of the speciation experiment since our recently-derived housefly populations are particularly vulnerable to inbreeding depression effects on mating behavior.     

Polygenic Mutation in Drosophila Melanogaster: The Causal Relationship of Bristle Number to Fitness

The association between sternopleural and abdominal bristle number and fitness in Drosophila melanogaster was determined for sublines of an initially highly inbred strain that were maintained by divergent artificial selection for 150 generations or by random mating for 180 generations. Replicate selection lines had more extreme bristle numbers than those that were maintained without artificial selection at the same census size for approximately the same number of generations. The average fitness, estimated by a single generation of competition against a compound autosome strain, was 0.17 for lines selected for high and low abdominal bristle numbers and 0.19 for lines selected for high and low sternopleural bristle number. The average fitness of unselected lines, 0.46, was significantly higher than that of the selection lines. The fitnesses and the relationships of bristle number to fitness in progeny of all possible crosses of high X high (H X H), high X low (H X L) and low X low (L X L) selection lines were examined to determine whether the observed intermediate optima were caused by direct stabilizing selection on bristle number or by apparent stabilizing selection mediated through deleterious pleiotropic fitness effects of mutations affecting bristle number. Although bristle number was nearly additive for progeny of H X H, H X L and L X L crosses among sternopleural bristle selection lines, their mean fitnesses were not significantly different from each other, or from the mean fitness of the unselected lines, suggesting partly or completely recessive pleiotropic fitness effects cause apparent stabilizing selection. The average fitness of the progeny of H X H abdominal bristle selection lines was not significantly different from the fitness of unselected lines, but the mean fitness of the progeny of L X L crosses was not significantly different from that of the pure low lines. This is consistent with direct selection against low but not high abdominal bristle number, but the interpretation is confounded by variation in average degree of dominance for fitness (on average recessive in the high abdominal bristle selection lines and additive in the low abdominal bristle selection lines). Neither direct stabilizing selection nor pleiotropy, therefore, can account for all the observations.     

Inbreeding depression and male-mating behavior inDrosophila melanogaster

There have been relatively few studies designed to investigate the effects of inbreeding on behavioral traits. To study this phenomenon, five experimental lines ofDrosophila melanogaster made isogenic for chromosome 2 were evaluated for their male-mating ability and, subsequently, male courtship behavior. All lines showed significant reductions in overall mating ability, and males from all of these lines displayed impaired mating behavior, with two lines displaying particularly aberrant courtship patterns. Line 16 displayed an inability to successfully initiate copulation following successful courtship, while line 17 displayed significant reduction in locomotor activity, resulting in virtually no successful courtship or copulatory activity. The implications of these findings for competitive mating ability in wildDrosophila populations are presented. Further, the importance of mating success as a fitness component in the management of potentially highly inbred populations of endangered species is discussed.     

Direct and correlated responses to artificial selection on male mating frequency in the stalk-eyed fly Cyrtodiopsis dalmanni

Traditionally it was thought that fitness-related traits such as male mating frequency, with a history of strong directional selection, should have little additive genetic variance and thus respond asymmetrically to bidirectional artificial selection. However, recent findings and theory suggest that a balance between selection for increased male mating frequency and opposing selection pressures on physiologically linked traits will cause male mating frequency to have high additive genetic variation and hence respond symmetrically to selection. We tested these hypotheses in the stalk-eyed fly, Cyrtodiopsis dalmanni, in which males hold harems comprising many females and so have the opportunity to mate at extremely high frequencies. We subjected male stalk-eyed flies to artificial selection for increased ('high') and decreased ('low') mating frequency in the presence of ecologically realistic, high numbers of females. High line males mated significantly more often than control or low line males. The direct response to selection was approximately symmetric in the high and low lines, revealing high additive genetic variation for, and no significant genetic constraints on, increased male mating frequency in C. dalmanni. In order to investigate trade-offs that might constrain male mating frequency under natural conditions we examined correlated responses to artificial selection. We measured accessory gland length, testis length and eyespan after 7 and 14 generations of selection. High line males had significantly larger accessory glands than low line males. No consistent correlated responses to selection were found in testis length or eyespan. Our results suggest that costs associated with the production and maintenance of large accessory glands, although yet to be identified, are likely to be a major constraint on mating frequency in natural populations of C. dalmanni.     

Mating speed and the interplay between female and male courtship responses inDrosophila melanogaster (Diptera: Drosophilidae)

The objective of this study was to compare measures of general activity and sexual behavior for various genotypes within a strain of Drosophila melanogaster, which had known differences in mating speed. Three inbred lines of D. melanogaster differed significantly in mating speed when tested in female-choice and in single-pair experiments. Analyses of locomotor activity and sexual activity of females and males revealed no significant differences between the inbred lines. An analysis of the interplay between female and male courtship behaviors enabled the examination of signal-response differences between the inbred lines. The inbred lines with intermediate and slow mean mating speed showed a decreased number of significant transitions between female and male behavioral responses. This decrease was more severe in the slow mating line. Further, the intermediate- and slow-mating females and males displayed courtship responses toward signals of the opposite sex that were different from those of the fastmating line. Models of the relationship between behavioral activity and mating speed in Drosophila are discussed and a different explanation for variation in mating speed among the three inbred lines is considered.     

Quantitative Genetics of Sperm Precedence in Drosophila Melanogaster

To assess the genetic basis of sperm competition under conditions in which it occurs, I estimated additive, dominance, homozygous and environmental variance components, the effects of inbreeding, and the weighted average dominance of segregating alleles for two measures of sperm precedence in a large, outbred laboratory population. Both first and second male precedence show significant decline on inbreeding. Second male precedence demonstrates significant dominance variance and homozygous genetic variance, but the additive variance is low and not significantly different from zero. For first male precedence, the variance among homozygous lines is again significant, and dominance variance is larger than the additive variance, but is not statistically significant. In contrast, male mating success and other fitness components in Drosophila generally exhibit significant additive variance and little or no dominance variance. Other recent experiments have shown significant genotypic variation for sperm precedence and have associated it with allelic variants of accessory-gland proteins. The contrast between sperm precedence and other male fitness traits in the structure of quantitative genetic variation suggests that different mechanisms may be responsible for the maintenance of variation in these traits. The pattern of genetic variation and inbreeding decline shown in this experiment suggests that one or a few genes with major effects on sperm precedence may be segregating in this population.     

Population and behaviour genetics of Drosophila ananassae

Drosophila ananassae is a cosmopolitan and domestic species. It occupies a nuique status among the Drosophila species due to certain peculiarities in its genetic behaviour. The most unusual feature of this species is spontaneous male recombination in appreciable frequency. The present review summarises the work done on population and behaviour genetics of D. ananassae from India. Population dynamics of three cosmopolitan inversions has been studied in Indian population of D. ananassae and it is evident from the results that there is a considerable degree of genetic divergence at the level of inversion polymorphism. In general, the populations from south India show more differentiation than those from the north. These three cosmopolitan inversions, which are coextensive with the species, exhibit heterosis. Interracial hybridization does not lead to beaakdown of heterosis, which suggests that evidence for coadaptation is lacking in geographic populations of D. ananassae. Heterosis appears to be simple luxuriance rather than populational heterosis (coadaptation). Unlinked inversions occur in random associations, indicating no interchromosomal interactions. However, two inversions of the third chromosome often show strong linkage disequilibrium in laboratory populations, which is due to epistatic gene interaction and suppression of crossing-over. Genetic variations for certain allozyme polymorphism and sternoleural bristle phenotypes in Indian populations of D. ananassae have also been observed.A number of investigations have also been carried out on certain aspects of behaviour genetics of Indian D. ananassae. There is evidence for sexual isolation within D. ananassae. Significant variations in mating propensity of several isofemale strains, inversion karyotypes, the diminishing effects of certain mutations on sexual activity of males and positive response to selection for high and low mating propensity provide evidence for genetic control of sexual behaviour in D. ananassae. Males contribute more to variation and thus are more subject to intra-sexual selection than females. Evidence for rare male mating advantage has also been presented. Geographic strains of D. ananassae show variation with respect to oviposition site preference. The results of studies on pupation site preference, which is an important component of larval behaviour, suggest that larval pupation behaviour in D. ananassae is under polygenic control with a substantial amount of additive genetic variation.     

The role of female dominance hierarchies in the mating behaviour of mosquitofish

While studies of sexual selection focus primarily on female choice and male-male competition, males should also exert mate choice in order to maximize their reproductive success. We examined male mate choice in mosquitofish, Gambusia holbrooki, with respect to female size and female dominance. We found that the number of mating attempts made by a male was predicted by the dominance rank of females in a group, with dominant females attracting more mating attempts than subordinates. The number of mating attempts made by males was independent of the female size. The observed bias in the number of mating attempts towards dominant females may be driven either by straightforward male mate choice, since dominance and female fecundity are often closely related, or via the dominant females mediating male mating behaviour by restricting their access to subordinate females.     

Sexual Selection in Black Morph Girardinus metallicus (Pisces: Poeciliidae): Females Can Spot a Winner (But We Cannot)

Male–male competition may interfere with the ability of females to choose mates by interrupting courtship or by favoring highly aggressive males who may damage females during mating attempts. Alternatively, females may benefit by mating with dominant males, and female choice and male–male competition may therefore act in unison. The same traits, including aggressiveness, may indicate male quality to females and to rivals. We investigated sexual selection in the black morph of the endemic Cuban poeciliid fish, Girardinus metallicus, to ascertain the links between morphological and behavioral traits and success in intra‐ and intersexual selection. Males conspicuously exhibit their black ventral surface and gonopodium to females during courtship. Dichotomous choice tests revealed female association preferences for certain males, and those same males were more successful in monopolizing access to females when the fish were allowed to directly interact. Dominant males followed, courted, and copulated with females more than subordinate males within a pair, and it appears that females could either assess dominance based on cues we did not measure, or could influence subsequent mating success by their behavior during the dichotomous choice trials. There was an interaction between black status (i.e., whether the male in each pair had more or less ventral black coloration than the other male in that pair) and dominance, such that low‐black dominant males courted early and then shifted to following females, whereas high‐black dominant males courted far more later in the observation period. These results hint at the importance for sexual selection of the interplay between a static morphological trait (black coloration) and a dynamic behavioral trait (aggressiveness), but the functional significance of the courtship display remains a mystery.     

Population bottlenecks increase additive genetic variance but do not break a selection limit in rain forest Drosophila

According to neutral quantitative genetic theory, population bottlenecks are expected to decrease standing levels of additive genetic variance of quantitative traits. However, some empirical and theoretical results suggest that, if nonadditive genetic effects influence the trait, bottlenecks may actually increase additive genetic variance. This has been an important issue in conservation genetics where it has been suggested that small population size might actually experience an increase rather than a decrease in the rate of adaptation. Here we test if bottlenecks can break a selection limit for desiccation resistance in the rain forest-restricted fly Drosophila bunnanda. After one generation of single-pair mating, additive genetic variance for desiccation resistance increased to a significant level, on average higher than for the control lines. Line crosses revealed that both dominance and epistatic effects were responsible for the divergence in desiccation resistance between the original control and a bottlenecked line exhibiting increased additive genetic variance for desiccation resistance. However, when bottlenecked lines were selected for increased desiccation resistance, there was only a small shift in resistance, much less than predicted by the released additive genetic variance. The small selection response in the bottlenecked lines was no greater than that observed in the control lines. Thus bottlenecks might produce a statistically detectable change in additive genetic variance but this change has no impact on the response to selection.     

A test of speciation via sexual selection on female preferences

Sexual selection for divergent female preferences has been proposed to stimulate speciation. We tested this basic model by selecting for divergence in the courtship repertoire of the house fly Musca domestica L. Specifically, we subjected replicate strains to artificial selection for differentiation along the first two principal components of the phenotypic intercorrelation structure of five courtship traits. Highly significant differentiation in courtship repertoire resulted, and the magnitude of the selection response was highest along the first principal component (representing the ‘size’, or general intensity, of courtship). Videotaped matings of the crosses between divergent lines (i.e. males of one strain mating with females from a different line) showed that the selection responses in the intensities of male performances were due to shifts in female preferences. In particular, the males were able to accommodate the demands of ‘foreign’ females (as well as their own) in the no-choice situation (i.e. only one male and one female per mating chamber). In contrast to this plasticity of the males, the females were consistent in their differential resistance responses, regardless of the type of male involved in the courtship. Multiple-choice mate choice tests revealed significant reproductive isolation among some lines, although the effect was asymmetrical. The patterns of nonrandom mating were largely due to females from more genetically healthy lines (i.e. with overall high mating propensity) discriminating against males from populations with more inbreeding depression. We suggest that the inability to achieve true (symmetrical) reproductive isolation could have been due to low evolutionary potential in the ‘shape’ of courtship, as defined by the second principal component. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

Response to Selection for Mating Speed and Changes in Gene Arrangement Frequencies in Descendants from a Single Population of DROSOPHILA PSEUDOOBSCURA

Heritability estimates, based on 19 generations of selection for fast and slow mating speed, were not significantly different from zero at the 0.05 level in any replicate of selected lines in a population of flies descended from the Mather population in California. Only the combined heritability estimate of approximately 2% was significant. This indicated that very little additive genetic variance was present in the base population and that strong directional selection for rapid mating may have occurred in the previous history of the local population at Mather and/or during its many generations of laboratory propagation. Frequencies of third chromosome gene arrangements were monitored during the course of selection. Balancing selection, unrelated to that imposed for mating speed, and genetic drift appeared to be the major factors causing changes in chromosome frequencies. Present differences in adaptive value of third chromosome variants in nature may be associated with nonadditive effects on mating speed, as well as effects on other components of fitness.