GENETIC CORRELATION BETWEEN A FEMALE MATING PREFERENCE AND THE PREFERRED MALE CHARACTER IN SEAWEED FLIES (COELOPA FRIGIDA)

The mating preferences of female seaweed flies Coelopa frigida were determined by observing their acceptance or rejection of males of known size. The inversion karyotype of both males and females was also determined. Females exhibited a preference to mate with large males, and evidence is presented that a genetic correlation exists between the female preference and the preferred trait. Females carrying the inversion karyotype associated with large male size showed a strong preference for large males; females carrying the inversion associated with small male size also exhibited a preference for large males, but it was significantly less strong. This finding suggests that a Fisherian process may be operating.     

FEMALE PREFERENCE FOR MALE COURTSHIP EFFORT CAN DRIVE THE EVOLUTION OF MALE MATE CHOICE

The evolution of male mate choice is constrained by costs of choice in species with a male‐biased operational sex ratio (OSR). Previous theoretical studies have shown that significant benefits of male choice are required, for example, by mating with more fecund females, in order for these costs to be offset and a male preference to spread. In a series of population genetic models we show the novel effect that male mating preference, expressed as a bias in courtship, can spread when females prefer, and thus are more likely to mate with, males who court more. We explore two female preference functions for levels of male courtship, one representing a threshold and the other a weighted female preference. The basic finding generally holds for both preference functions. However, the preference function greatly affects the spread of a male preference allele after the addition of competing males who can court more in total. Our results thus stress that a thorough understanding of the response of females to male courtship is a critical component to understanding male preference evolution in polygynous species.     

IDENTIFICATION OF GENETICALLY LINKED FEMALE PREFERENCE AND MALE TRAIT

Genetic variation in male traits and the female preferences for those traits allows for the evolution of sexual behavior. Trait–preference combinations are thought to improve the effectiveness of runaway sexual selection within a species, and are considered necessary for the induction of divergence between species. Novel traits, or variants of existing traits, and their associated preferences in the opposite sex are more likely to be maintained if they are genetically linked in proximity on a chromosome (the genetic coupling hypothesis), yet there is little empirical evidence that this genetic linkage occurs. Here we show for the first time that natural genetic variation at a single‐linked region can induce both species‐specific female choosiness and the male trait they are discriminating against. We found this effect in two separate regions of the genome, demonstrating that this linkage may be common. In contrast, female choosiness and male unattractiveness could not be alleviated by a single region. The close linkage of these loci and the strength of their effect provide an evolutionary means by which this preference–trait combination could arise and be maintained, thus enabling a more rapid route for runaway sexual selection, and providing empirical evidence supporting the genetic coupling hypothesis.     

SEX DIFFERENCES IN MATE RECOGNITION AND CONSPECIFIC PREFERENCE IN SPECIES WITH MUTUAL MATE CHOICE

Sexual isolation is often assumed to arise because choosy females recognize and reject heterospecific males as mates. Yet in taxa in which both males and females are choosy, males might also recognize and reject heterospecific females. Here, we asked about the relative contribution of the sexes to the strong sexual isolation found in limnetic–benthic species pairs of threespine sticklebacks, which show mutual mate choice. We asked whether males and females of the two species recognize conspecifics and also prefer to mate with them. We found evidence for mate recognition by both sexes but only females prefer conspecifics. The nature of male courtship depended on which species of female they were courting, indicating that males recognized conspecific females and differentiated them from heterospecifics. However, males courted both species of females with equal vigor and changed courtship in a manner that would increase the chance of mating with heterospecifics. Females both recognized conspecifics and strongly preferred them. They responded very little to heterospecific male courtship and almost never mated with them. Therefore, males are likely to undermine sexual isolation, but females uphold it. Despite mutual mate choice and mate recognition in both sexes, females are primarily responsible for sexual isolation in these taxa.     

BOTH MALE AND FEMALE SEXUAL ORNAMENTS REFLECT OFFSPRING PERFORMANCE IN A FISH

Secondary sexual characters are often expressed in both sexes (mutual ornamentation), but are less often studied simultaneously. We studied the adaptive signaling function of male and female ornamentation in a mutually ornamented fish, the whitefish Coregonus lavaretus. In an experimental design in which nongenetic environmental effects were minimized, we found that highly ornamented females, males, and their parental combinations had offspring with better swimming performance and predator‐avoidance ability than less ornamented individuals or combinations. Furthermore, highly ornamented females had larger offspring that also had higher yolk volume than less ornamented individuals. Offspring swimming performance was not dependent on offspring size and was only weakly affected by yolk volume, which suggest that swimming performance and measured morphological traits are independent fitness measures. In conclusion, mutual ornamentation of whitefish may signal the quality of individuals in both sexes, which may indicate ongoing directional selection for these ornamental traits. However, offspring fitness traits were also dependent on parental combination, which suggests that genetic compatibility effects may weaken the directional selection and the indicator value of the ornamentation.     

GENETIC,ENVIRONMENTAL, AND CONDITION-DEPENDENT EFFECTS ON FEMALE AND MALE ORNAMENTATION IN THE BARN OWL TYTO ALBA

Secondary sexual characters are thought to indicate individual quality. Expression of sex-limited traits in an extravagant state may require both the underlying genes and the available nutrient resources. The assessment of the relative contribution of genes, environment, and body condition is relevant for understanding to that extent the extravagant trait may signal genotypic or phenotypic quality of the individual. In birds, usually only the males are ornamented. In the barn owl, Tyto alba, both females and males display sex-limited plumage traits. Males are commonly lighter colored and females spottier. In an experiment with combined cross-fostering and brood size manipulation we determined the relative contribution of genes, environment, and body condition to the variation in plumage coloration and plumage spottiness. The partial cross-fostering experiment tested the relative importance of shared genes and a shared environment for the resemblance of related birds. Siblings raised in different nests converged toward similar trait values, offspring resembled the true but not the foster parents, and plumage traits of unrelated nestlings sharing the same nest were not correlated. Results were not inflated by maternal effects detectable in the mother's phenotype, because middaughter to mother resemblance was not higher than midson to father resemblance. This suggests that plumage coloration and spottiness are largely genetically inherited traits, and that the rearing environment does not have a strong impact on the expression of these traits. To further investigate whether the two sex-limited traits are condition dependent, brood sizes were manipulated. Enlargement or reduction of broods by two nestlings resulted in lower and higher body mass of nestlings, respectively. However, nestlings raised in enlarged or reduced broods did not show either a significantly darker or lighter or a more or less spotted plumage. We did not detect any genotype-by-environment interaction. In conclusion, simultaneous cross-fostering and brood size manipulation demonstrate that additive genetic variance for plumage coloration and spottiness is maintained and that both the rearing environment and body condition do not account for a large proportion of the phenotypic variance in female and male ornamentations.     

THE INTERPLAY BETWEEN LOCAL ECOLOGY,DIVERGENT SELECTION,AND GENETIC DRIFT IN POPULATION DIVERGENCE OF A SEXUALLY ANTAGONISTIC FEMALE TRAIT

Genetically polymorphic species offer the possibility to study maintenance of genetic variation and the potential role for genetic drift in population divergence. Indirect inference of the selection regimes operating on polymorphic traits can be achieved by comparing population divergence in neutral genetic markers with population divergence in trait frequencies. Such an approach could further be combined with ecological data to better understand agents of selection. Here, we infer the selective regimes acting on a polymorphic mating trait in an insect group; the dorsal structures (either rough or smooth) of female diving beetles. Our recent work suggests that the rough structures have a sexually antagonistic function in reducing male mating attempts. For two species (Dytiscus lapponicus and Graphoderus zonatus), we could not reject genetic drift as an explanation for population divergence in morph frequencies, whereas for the third (Hygrotus impressopunctatus) we found that divergent selection pulls morph frequencies apart across populations. Furthermore, population morph frequencies in H. impressopunctatus were significantly related to local bioclimatic factors, providing an additional line of evidence for local adaptation in this species. These data, therefore, suggest that local ecological factors and sexual conflict interact over larger spatial scales to shape population divergence in the polymorphism.     

ORIGIN AND MAINTENANCE OF A FEMALE MATING PREFERENCE

We investigated the role of maintenance and origin of female mating preferences in three species of fish. Poecilia latipinna and P. mexicana are sexual species that hybridized to form the gynogenetic clonal P. formosa, which reproduces asexually but requires sperm to initiate embryogenesis. We demonstrate that all three species display almost identical and statistically indistinguishable preferences for large males. Although processes of good genes, runaway sexual selection, and direct selection could maintain preferences in the sexual species, good genes and runaway sexual selection are unlikely to operate in the asexual species. Furthermore, we found that the most likely direct selection benefit, an increase in fecundity, can also be excluded in the gynogens. We conclude that the most parsimonious explanation for this P. formosa preference is that it was inherited from the parental species and is maintained without forces generated by good genes, runaway selection, or direct selection for increased fecundity. This preference may be maintained because of pleiotropic effects (e.g., sensory bias) or mate searching costs.     

INCIPIENT SPECIATION BY SEXUAL ISOLATION IN DROSOPHILA MELANOGASTER: VARIATION IN MATING PREFERENCE AND CORRELATION BETWEEN SEXES

Genetic divergence for characters pertaining to reproductive isolation is of considerable interest in evolutionary biology. Since most studies concentrate on sibling species (for recent reviews, see Wu et al. 1996), we would like to know how much genetic variation exists between populations that are at an incipient stage of speciation. To answer this question, we have begun measuring variations in mating preference among natural isolates of Drosophila melanogaster, represented by the cosmopolitan and Zimbabwe sexual races. We quantify the variation in mating preference and success in both sexes by using a multiple-choice design and an index that is suited to cases of strong asymmetry in mate choice. Different designs and indices for measuring sexual isolation are also discussed. These sexual traits are entirely genetically determined. Surveying four populations in southern Africa and additional cosmopolitan lines, we observe extensive genetic variation in sexual characters as well as strong correlation between sexes. The populations are highly differentiated and represent various stages of evolution between the African and the cosmopolitan type of sexual behaviors. The genetic variation and correlation for these sexual characters coupled with their geographical pattern have interesting implications for models of speciation by sexual selection.     

FEMALE AND MALE GENETIC EFFECTS ON OFFSPRING PATERNITY: ADDITIVE GENETIC (CO)VARIANCES IN FEMALE EXTRA‐PAIR REPRODUCTION AND MALE PATERNITY SUCCESS IN SONG SPARROWS (MELOSPIZA MELODIA)

Ongoing evolution of polyandry, and consequent extra‐pair reproduction in socially monogamous systems, is hypothesized to be facilitated by indirect selection stemming from cross‐sex genetic covariances with components of male fitness. Specifically, polyandry is hypothesized to create positive genetic covariance with male paternity success due to inevitable assortative reproduction, driving ongoing coevolution. However, it remains unclear whether such covariances could or do emerge within complex polyandrous systems. First, we illustrate that genetic covariances between female extra‐pair reproduction and male within‐pair paternity success might be constrained in socially monogamous systems where female and male additive genetic effects can have opposing impacts on the paternity of jointly reared offspring. Second, we demonstrate nonzero additive genetic variance in female liability for extra‐pair reproduction and male liability for within‐pair paternity success, modeled as direct and associative genetic effects on offspring paternity, respectively, in free‐living song sparrows (Melospiza melodia). The posterior mean additive genetic covariance between these liabilities was slightly positive, but the credible interval was wide and overlapped zero. Therefore, although substantial total additive genetic variance exists, the hypothesis that ongoing evolution of female extra‐pair reproduction is facilitated by genetic covariance with male within‐pair paternity success cannot yet be definitively supported or rejected either conceptually or empirically.     

MALE MATE CHOICE AND THE EVOLUTION OF FEMALE PLUMAGE COLORATION IN THE HOUSE FINCH

The house finch (Carpodacus mexicanus) is a sexually dichromatic passerine in which males display colorful plumage and females are generally drab brown. Some females, however, have a subdued version of the same pattern of ornamental coloration seen in males. In previous research, I found that female house finches use male coloration as an important criterion when choosing mates and that the plumage brightness of males is a reliable indicator of male nest attentiveness. Male house finches invest substantially in the care of young and, like females, stand to gain by choosing high-quality mates. I therefore hypothesized that a female's plumage brightness might be correlated with her quality and be the basis for male mate choice. In laboratory mate choice experiments, male house finches showed a significant preference for the most brightly plumaged females presented. Observations of a wild population of house finches, however, suggest that female age is the primary criterion in male choice and that female plumage coloration is a secondary criterion. In addition, yearling females tended to have more brightly colored plumage than older females, and there was no relationship between female plumage coloration and overwinter survival, reproductive success, or condition. These observations fail to support the idea that female plumage coloration is an indicator of individual quality. Male mate choice for brightly plumaged females may have evolved as a correlated response to selection on females to choose brightly colored males.     

GENETIC CORRELATIONS BETWEEN LIFE-HISTORY AND BEHAVIORAL TRAITS CAN CAUSE REPRODUCTIVE ISOLATION

Reproductive isolation may often evolve as an indirect (pleiotropic) consequence of populations adapting to different environments or habitats. For example, niches that are temporally or seasonally offset can select for organisms with different developmental characteristics. These developmental differences can inadvertently cause reproductive isolation by a variety of means including shifts in mating activity patterns. Here, we show a genetic correlation between a life-history trait (developmental period) and a behavioral trait (time of mating) that causes significant premating isolation in the melon fly, Bactrocera cucurbitae (Diptera: Tephritidae). Fly lines selected for short and long developmental periods differ in their preferred times of mating during the evening. This difference translates into significant prezygotic isolation, as measured by mate choice tests. If the time of mating between two populations differed more than one hour, the isolation index was significantly higher than zero. These indicate that premating isolation can be established if the developmental period is divergently selected for. If such genetic correlations are ubiquitous in many organisms, multifarious divergent selection for life-history traits would often accelerate the evolution of reproductive isolation. We speculate that reproductive isolation may have been evolved via genetic correlations among time-related traits, for example, developmental period and time of mating, as in other organisms.     

HERITABILITIES OF DOMINANCE-RELATED TRAITS IN MALE BANK VOLES (CLETHRIONOMYS GLAREOLUS)

A number of studies have shown that in several animal species females prefer dominant males as mating partners, but fewer attempts have been made to measure possible indirect benefits of this choice. One reason for this may be that, even though dominance is a widely used concept, the definition of dominance still remains controversial Furthermore, defining and measuring the heritability of social behaviors is problematic because they are not individual traits but, by definition, involve interactions between at least two individuals. In this study we estimated heritabilities and coefficients of additive genetic variances (CV_A) for male traits that are closely associated with dominance and female mating preferences in bank voles (Clethrionomys glareolus). The heritability values were estimated using father-offspring regression. All heritability estimates were relatively high ranging from 0.531 (urine marking) to 0.767 (preputial glands). The CV_A-values indicated high levels of additive genetic variance especially in the characters most closely related to dominance: the weight of preputial glands and urine marking behavior. All phenotypic correlations among the traits measured were significantly positive and the genetic correlations were of similar magnitude as the corresponding phenotypic counterparts. Even though heritabilities may be lower in the natural environment than under controlled laboratory conditions, our results suggest that characters closely related to dominance may be at least partly genetically determined.     

SEX-LINKAGE OF SEXUALLY ANTAGONISTIC GENES IS PREDICTED BY FEMALE, BUT NOT MALE, EFFECTS IN BIRDS

Evolutionary theory predicts that sexually antagonistic loci will be preferentially sex-linked, and this association can be empirically testes with data on sex-biased gene expression with the assumption that sex-biased gene expression represents the resolution of past sexual antagonism. However, incomplete dosage compensating mechanisms and meiotic sex chromosome inactivation have hampered efforts to connect expression data to theoretical predictions regarding the genomic distribution of sexually antagonistic loci in a variety of animals. Here we use data on the underlying regulatory mechanism that produce expression sex-bias to test the genomic distribution of sexually antagonistic genes in chicken. Using this approach, which is free from problems associated with the lack of dosage compensation in birds, we show that female-detriment genes are significantly overrepresented on the Z chromosome, and female-benefit genes underrepresented. By contrast, male-effect genes show no over- or underrepresentation on the Z chromosome. These data are consistent with a dominant mode of inheritance for sexually antagonistic genes, in which male-benefit coding mutations are more likely to be fixed on the Z due to stronger male-specific selective pressures. After fixation of male-benefit alleles, regulatory changes in females evolve to minimize antagonism by reducing female expression.     

GEOGRAPHIC VARIATION IN FEMALE PREFERENCES FOR MALE TRAITS IN POECILIA RETICULATA

We examined the preferences of female guppies (Poecilia reticulata) from 11 localities in Trinidad with respect to male color-pattern elements, body shape and size, and overall color and brightness contrast. Females are on average more attracted to males from their own population than from alien populations, and populations appear to vary in the criteria used in female choice. Multiple-regression analysis suggests that mate-preference criteria vary among localities in intensity, sign, and the number of traits used. Although preference estimators and color-pattern parameters are unique to each population, only orange, black, and color contrast showed a correlation between degree of male trait and degree of preference for that trait. There is a clear effect of water color and a possible effect of predation intensity. The results are discussed in light of various models of sexual selection and the early stages of speciation.     

GENETIC VARIATION FOR FEMALE MATE DISCRIMINATION IN DROSOPHILA MELANOGASTER

Comparisons between the Canton-S and Tai-Y strains of Drosophila melanogaster (both wild type) revealed variation in female mate discrimination based on chemical courtship signals present as hydrocarbons on the male cuticle. Mating tests indicated that 7-tricosene, which is the primary hydrocarbon on the Canton-S male cuticle but is nearly absent from Tai-Y, was a significant component of the signal. The discrimination was asymmetrical in that Canton-S females clearly distinguished between the two types of males in no-choice tests, but Tai-Y females did not. F₁ females expressed an intermediate ability to discriminate, and female progeny of backcrosses expressed a mating phenotype very similar to that of the parental strain to which the backcross was made. Analysis of independent effects from the X and both major autosomes indicated that the discrimination is controlled by gene(s) on chromosome 3.     

DIRECT AND INDIRECT SEXUAL SELECTION AND QUANTITATIVE GENETICS OF MALE TRAITS IN GUPPIES (POECILIA RETICULATA)

Abstract.— The ornamentation and displays on which sexual attractiveness and thus mating success are based may be complex and comprise several traits. Predicting the outcome of sexual selection on such complex phenotypes requires an understanding of both the direct operation of selection on each trait and the indirect consequences of selection operating directly on genetically correlated traits. Here we report the results of a quantitative genetic analysis of the ornamentation, sexual attractiveness, and mating success of male guppies (Poecilia reticulata). We analyze male ornamentation both from the point of view of single ornamental traits (e.g., the area of each color) and of composite measures of the way the entire pattern is likely to be perceived by females (e.g., the mean and contrast in chroma). We demonstrate that there is substantial additive genetic variation in almost all measures of male ornamentation and that much of this variation may be Y linked. Attractiveness and mating success are positively correlated at the phenotypic and genetic level. Orange area and chroma, the area of a male's tail, and the color contrast of his pattern overall are positively correlated with attractiveness and/or mating success at the phenotypic and genetic levels. Using attractiveness and mating success as measures of fitness, we estimate gradients of linear directional sexual selection operating on each male trait and use equations of multivariate evolutionary change to predict the response of male ornamentation to this sexual selection. From these analyses, we predict that indirect selection may have important effects on the evolution of male guppy color patterns.     

QUANTITATIVE GENETIC ANALYSIS OF DIVERGENCE IN MALE SECONDARY SEXUAL TRAITS BETWEEN DROSOPHILA SIMULANS AND DROSOPHILA MAURITIANA

The sibling species Drosophila simulans and D. mauritiana differ significantly in a number of male secondary sexual traits, providing an ideal system for genetic analysis of interspecific morphological divergence. In the experiment reported here, F₁ hybrids from a cross of two inbred lines were backcrossed in both directions and about 200 flies from each backcross were scored for several traits (bristle numbers and cuticle areas), as well as 18 markers distributed throughout the genome. Each trait was analyzed by composite interval mapping to identify quantitative trait loci (QTL) and estimate their effects. For each trait, from one to eight loci were detected, with more divergent traits showing evidence for greater numbers of QTL. Estimates of additive effects varied widely, with a range of 0.4 to 4.1 environmental standard deviation units and an average of 2.2 units. There was substantial evidence for nonadditive effects, since the magnitude of estimates often differed significantly between the two backcrosses. The sign of the estimated effect differed among QTL for bristle traits, but not for cuticle area traits, suggesting that these two types of trait may have undergone different types of selection. Finally, several similarities were found between different traits in the estimated positions of QTL, suggesting that pleiotropy and/or linkage of QTL may have been important in the evolution of these traits.     

GENETIC CONSTRAINTS ON THE INDEPENDENT EVOLUTION OF MALE AND FEMALE REPRODUCTIVE CHARACTERS IN THE TRISTYLOUS PLANT LYTHRUM SALICARIA

Here we test whether the potential exists for the independent evolution of allocation to male, female, and attractive functions within a flower. We employed half-sib and parent-offspring regression methods in the tristylous plant Lythrum salicaria to determine whether there is additive genetic variation for characters important to male and female reproductive success and whether genetic correlations could constrain the independent evolution of male and female function. Although significance levels were not consistent among morph types or between populations, there were significant narrow-sense heritabilities for several traits including stamen mass, pistil mass, perianth mass, petal length, and calyx length. Traits that might be under strong stabilizing selection to promote specific pollen transfer, such as stamen and style lengths, had little heritable variation. In the majority of cases in which heritable variation was present, there were positive genetic correlations among floral traits. A strong positive genetic correlation appeared between stamen and pistil mass in the short-styled morph from one of the populations studied. This suggests that selection might not be able to act independently on biomass allocation to male and female flower parts. No evidence of negative genetic correlations appeared that would suggest trade-offs and that could augment a selection response towards sexual specialization. The observed positive correlations could be explained if we consider the “functional architecture” that underlies the covariance structure. If there is more covariance generated by pleiotropic loci controlling overall flower size than at loci controlling male versus female allocation, it could result in the observed positive covariance. At the phenotypic level, we did find significant negative partial correlations between male and female traits when flower size was controlled, but these trade-offs were among rather than within morphs.     

EVOLUTION OF MULTIPLE KINDS OF FEMALE SPERM-STORAGE ORGANS IN DROSOPHILA

Females of all species belonging to the family Drosophilidae have two kinds of sperm-storage organs: paired spherical spermathecae and a single elongate tubular seminal receptacle. We examined 113 species belonging to the genus Drosophila and closely allied genera and describe variation in female sperm-storage organ use and morphology. The macroevolutionary pattern of organ dysfunction and morphological divergence suggests that ancestrally both kinds of organs stored sperm. Loss of use of the spermathecae has evolved at least 13 times; evolutionary regain of spermathecal function has rarely if ever occurred. Loss of use of the seminal receptacle has likely occurred only once; in this case, all descendant species possess unusually elaborate spermathecae. Data further indicate that the seminal receptacle is the primary sperm-storage organ in Drosophila. This organ exhibits a pattern of strong correlated evolution with the length of sperm. The evolution of multiple kinds of female sperm-storage organs and the rapidly divergent and correlated evolution of sperm and female reproductive tract morphology are discussed.