Adult fitness consequences of sexual selection in Drosophila melanogaster

Few experiments have demonstrated a genetic correlation between the process of sexual selection and fitness benefits in offspring, either through female choice or male competition. Those that have looked at the relationship between female choice and offspring fitness have focused on juvenile fitness components, rather than fitness at later stages in the life cycle. In addition, many of these studies have not controlled for possible maternal effects. To test for a relationship between sexual selection and adult fitness, we carried out an artificial selection experiment in the fruit fly, Drosophila melanogaster. We created two treatments that varied in the level of opportunity for sexual selection. Increased opportunity for female choice and male competition was genetically correlated with an increase in adult survivorship, as well as an increase in male and female body size. Contrary to previous, single-generation studies, we did not find an increase in larval competitive ability. This study demonstrates that mate choice and/or male–male competition are correlated with an increase in at least one adult fitness component of offspring.

Incipient speciation by sexual isolation in Drosophila: Concurrent evolution at multiple loci

Drosophila melanogaster from Zimbabwe and nearby regions shows strong but asymmetric sexual isolation from its cosmopolitan counterparts. By creating stable chromosome-substitution lines, earlier studies were able to show that the two major autosomes have very large effects on both male mating success and female mating preference. In this study, we genetically dissect this sexual isolation by recombination analysis between a whole-chromosome substitution line (which carries a Zimbabwe-derived third chromosome) and a strain with seven visible markers on that chromosome. Four loci are responsible for male mating success and three others are found to control female mating preference. Because male and female traits are not closely linked, their strong association among isofemale lines is most likely a reflection of sexual selection in nature. The results suggest that a large number of behavioral loci may evolve concurrently in the incipient stage of speciation before other aspects of reproductive isolation (such as hybrid sterility) have become evident. The results shed light on the population genetic processes underlying the formation of nascent species, as well as modes of speciation.

Possible ecological risks of transgenic organism release when transgenes affect mating success: Sexual selection and the Trojan gene hypothesis

Widespread interest in producing transgenic organisms is balanced by concern over ecological hazards, such as species extinction if such organisms were to be released into nature. An ecological risk associated with the introduction of a transgenic organism is that the transgene, though rare, can spread in a natural population. An increase in transgene frequency is often assumed to be unlikely because transgenic organisms typically have some viability disadvantage. Reduced viability is assumed to be common because transgenic individuals are best viewed as macromutants that lack any history of selection that could reduce negative fitness effects. However, these arguments ignore the potential advantageous effects of transgenes on some aspect of fitness such as mating success. Here, we examine the risk to a natural population after release of a few transgenic individuals when the transgene trait simultaneously increases transgenic male mating success and lowers the viability of transgenic offspring. We obtained relevant life history data by using the small cyprinodont fish, Japanese medaka (Oryzias latipes) as a model. Our deterministic equations predict that a transgene introduced into a natural population by a small number of transgenic fish will spread as a result of enhanced mating advantage, but the reduced viability of offspring will cause eventual local extinction of both populations. Such risks should be evaluated with each new transgenic animal before release.

Is sexual selection and species recognition a continuum? Mating behavior of the stalk-eyed fly Drosophila heteroneura

If behavioral isolation between species can evolve as a consequence of sexual selection within a species, then traits that are both sexually selected and used as a criterion of species recognition by females should be identifiable. The broad male head of the Hawaiian picture-winged fly Drosophila heteroneura is a novel sexual dimorphism that may be sexually selected and involved in behavioral isolation from D. silvestris. We found that males with broad heads are more successful in sexual selection, both through female mate choice and through aggressive interactions. However, female D. heteroneura do not discriminate against hybrids on the basis of their head width. Thus, this novel trait is sexually selected but is not a major contributor to species recognition. Our methods should be applicable to other species in which behavioral isolation is a factor.

Sexual conflict promotes speciation in insects

Speciation rates among extant lineages of organisms vary extensively, but our understanding of the causes of this variation and, therefore, the processes of speciation is still remarkably incomplete. Both theoretical and empirical studies have indicated that sexual selection is important in speciation, but earlier discussions have focused almost exclusively on the potential role of female mate choice. Recent findings of postmating reproductive conflicts of interest between the sexes suggest a quite different route to speciation. Such conflicts may lead to perpetual antagonistic coevolution between males and females and may thus generate rapid evolutionary divergence of traits involved in reproduction. Here, we assess this hypothesis by contrasting pairs of related groups of insect species differing in the opportunity for postmating sexual conflict. Groups where females mate with many males exhibited speciation rates four times as high as in related groups where females mate only once. Our results not only highlight the general importance of postmating sexual selection in speciation, but also support the recent suggestion that sexual conflict is a key engine of speciation.

Transposable elements as sources of variation in animals and plants

A tremendous wealth of data is accumulating on the variety and distribution of transposable elements (TEs) in natural populations. There is little doubt that TEs provide new genetic variation on a scale, and with a degree of sophistication, previously unimagined. There are many examples of mutations and other types of genetic variation associated with the activity of mobile elements. Mutant phenotypes range from subtle changes in tissue specificity to dramatic alterations in the development and organization of tissues and organs. Such changes can occur because of insertions in coding regions, but the more sophisticated TE-mediated changes are more often the result of insertions into 5′ flanking regions and introns. Here, TE-induced variation is viewed from three evolutionary perspectives that are not mutually exclusive. First, variation resulting from the intrinsic parasitic nature of TE activity is examined. Second, we describe possible coadaptations between elements and their hosts that appear to have evolved because of selection to reduce the deleterious effects of new insertions on host fitness. Finally, some possible cases are explored in which the capacity of TEs to generate variation has been exploited by their hosts. The number of well documented cases in which element sequences appear to confer useful traits on the host, although small, is growing rapidly.

The contagion indicator hypothesis for parasite-mediated sexual selection.

Hamilton and Zuk [Hamilton, W. D. & Zuk, M. (1982) Science 218, 384-387] proposed that females choosing mates based on the degree of expression of male characters obtain heritable parasite resistance for their offspring. Alternatively, the "contagion indicator" hypothesis posits that females choose mates based on the degree of expression of male characters because the latter indicate a male's degree of infestation of parasites and thus the risk that choosing females and their offspring will acquire these parasites. I examined whether parasite transmittability affects the probability that parasite intensity and male mating success are negatively correlated in intraspecific studies of parasite-mediated sexual selection. When females risk infection of themselves or their future offspring as a result of mating with a parasitized male, negative relationships between parasite intensity and male mating success are significantly more likely to occur than when females do not risk such infection. The direct benefit to females of avoiding parasitic infection is proposed to lead to the linkage between variable secondary sexual characters and the intensity of transmittable parasites. The direct benefits of avoiding associatively transmittable parasites should be considered in future studies of parasite-mediated sexual selection.

Sexual isolation in Drosophila melanogaster: a possible case of incipient speciation.

It is generally believed that Drosophila melanogaster has no closely related species with which it can produce the viable and fertile hybrids that are essential for the genetic analysis of speciation. Following the recent report of molecular differentiation between a Zimbabwe, Africa, population and two United States populations, we provide evidence that strong sexual isolation exists between the D. melanogaster population in Zimbabwe and populations of other continents. In the presence of males of their own kind, females from most isofemale lines of Zimbabwe would not mate with males from elsewhere; the reciprocal mating is also significantly reduced, but to a lesser degree. The genes for sexual behaviors are apparently polymorphic in Zimbabwe and postmating reproductive isolation between this and other populations has not yet evolved. Whole chromosome substitutions indicate significant genetic contributions to male mating success by both major autosomes, whereas the X chromosome effect is too weak to measure. In addition, the relative mating success between hybrid and pure line males supports the interpretation of strong female choice. These observations suggest that we are seeing the early stages of speciation in this group and that it is driven by sexual selection. The genetic and molecular tractability of D. melanogaster offers great promise for the detailed analysis of this apparent case of incipient speciation.

Statistical analysis of shape through triangulation of landmarks: A study of sexual dimorphism in hominids

Two objects with homologous landmarks are said to be of the same shape if the configuration of landmarks of one object can be exactly matched with that of the other by translation, rotation/reflection, and scaling. In an earlier paper, the authors proposed statistical analysis of shape by considering logarithmic differences of all possible Euclidean distances between landmarks. Tests of significance for differences in the shape of objects and methods of discrimination between populations were developed with such data. In the present paper, the corresponding statistical methodology is developed by triangulation of the landmarks and by considering the angles as natural measurements of shape. This method is applied to the study of sexual dimorphism in hominids.

Polyploid formation created unique avenues for response to selection in Gossypium (cotton)

A detailed restriction fragment length polymorphism map was used to determine the chromosomal locations and subgenomic distributions of quantitative trait loci (QTLs) segregating in a cross between cultivars of allotetraploid (AADD) Gossypium hirsutum (“Upland” cotton) and Gossypium barbadense (“Sea Island,” “Pima,” or “Egyptian” cotton) that differ markedly in the quality and quantity of seed epidermal fibers. Most QTLs influencing fiber quality and yield are located on the “D” subgenome, derived from an ancestor that does not produce spinnable fibers. D subgenome QTLs may partly account for the fact that domestication and breeding of tetraploid cottons has resulted in fiber yield and quality levels superior to those achieved by parallel improvement of “A” genome diploid cottons. The merger of two genomes with different evolutionary histories in a common nucleus appears to offer unique avenues for phenotypic response to selection. This may partly compensate for reduction in quantitative variation associated with polyploid formation and be one basis for the prominence of polyploids among extant angiosperms. These findings impel molecular dissection of the roles of divergent subgenomes in quantitative inheritance in many other polyploids and further exploration of both “synthetic” polyploids and exotic diploid genotypes for agriculturally useful variation.

Rapid evolution in plant chitinases: Molecular targets of selection in plant-pathogen coevolution

Many pathogen recognition genes, such as plant R-genes, undergo rapid adaptive evolution, providing evidence that these genes play a critical role in plant-pathogen coevolution. Surprisingly, whether rapid adaptive evolution also occurs in genes encoding other kinds of plant defense proteins is unknown. Unlike recognition proteins, plant chitinases attack pathogens directly, conferring disease resistance by degrading chitin, a component of fungal cell walls. Here, we show that nonsynonymous substitution rates in plant class I chitinase often exceed synonymous rates in the plant genus Arabis (Cruciferae) and in other dicots, indicating a succession of adaptively driven amino acid replacements. We identify individual residues that are likely subject to positive selection by using codon substitution models and determine the location of these residues on the three-dimensional structure of class I chitinase. In contrast to primate lysozymes and plant class III chitinases, structural and functional relatives of class I chitinase, the adaptive replacements of class I chitinase occur disproportionately in the active site cleft. This highly unusual pattern of replacements suggests that fungi directly defend against chitinolytic activity through enzymatic inhibition or other forms of chemical resistance and identifies target residues for manipulating chitinolytic activity. These data also provide empirical evidence that plant defense proteins not involved in pathogen recognition also evolve in a manner consistent with rapid coevolutionary interactions.

Canine sexual dimorphism in Egyptian Eocene anthropoid primates: Catopithecus and Proteopithecus

Two very small late Eocene anthropoid primates, Catopithecus browni and Proteopithecus sylviae, from Fayum, Egypt show evidence of substantial sexual dimorphism in canine teeth. The degree of dimorphism suggests that these early anthropoids lived in social groups with a polygynous mating system and intense male–male competition. Catopithecus and Proteopithecus are smaller in estimated body size than any living primates showing canine dimorphism. The origin of canine dimorphism and polygyny in anthropoids was not associated with the evolution of large body size.

Genomic evidence for a complete sexual cycle in Candida albicans

Candida albicans is a diploid fungus that has become a medically important opportunistic pathogen in immunocompromised individuals. We have sequenced the C. albicans genome to 10.4-fold coverage and performed a comparative genomic analysis between C. albicans and Saccharomyces cerevisiae with the objective of assessing whether Candida possesses a genetic repertoire that could support a complete sexual cycle. Analyzing over 500 genes important for sexual differentiation in S. cerevisiae, we find many homologues of genes that are implicated in the initiation of meiosis, chromosome recombination, and the formation of synaptonemal complexes. However, others are striking in their absence. C. albicans seems to have homologues of all of the elements of a functional pheromone response pathway involved in mating in S. cerevisiae but lacks many homologues of S. cerevisiae genes for meiosis. Other meiotic gene homologues in organisms ranging from filamentous fungi to Drosophila melanogaster and Caenorhabditis elegans were also found in the C. albicans genome, suggesting potential alternative mechanisms of genetic exchange.

Traumatic insemination and sexual conflict in the bed bug Cimex lectularius

The bed bug, Cimex lectularius, has a unique mode of copulation termed “traumatic” insemination [Carayon, J. (1966) in Monograph of the Cimicidae, ed. Usinger, R. (Entomol. Soc. Am., Philadelphia), pp. 81–167] during which the male pierces the female's abdominal wall with his external genitalia and inseminates into her body cavity [Carayon, J. (1966) in Monograph of the Cimicidae, ed. Usinger, R. (Entomol. Soc. Am., Philadelphia), pp. 81–167]. Under controlled natural conditions, traumatic insemination was frequent and temporally restricted. We show for the first time, to our knowledge, that traumatic insemination results in (i) last-male sperm precedence, (ii) suboptimal remating frequencies for the maintenance of female fertility, and (iii) reduced longevity and reproductive success in females. Experimental females did not receive indirect benefits from multiple mating. We conclude that traumatic insemination is probably a coercive male copulatory strategy that results in a sexual conflict of interests.