THE EVOLUTION OF REVERSED SEXUAL DIMORPHISM IN SIZE IN MONOGAMOUS SPECIES OF BIRDS

Reversed sexual dimorphism in size (RSD) occurs in most species of several taxonomic groups of birds. The hypotheses proposed to explain this phenomenon are examined theoretically, using inequalities to state selection in the most rigorous possible terms. The most pertinent empirical evidence is also examined critically. Proponents of hypotheses on the evolution of RSD have failed to consider the genetic constraints on the evolution of dimorphism. Selection for dimorphism can act on only that small portion of the genetic determination of body size that is sex limited. In general, selection for body size is much more likely to lead to a similar change (e.g. larger) in both sexes than to dimorphism. The most popular hypotheses involve selection for size-related differences in foraging ability. It is unlikely that there is variation in size-related foraging differences available for selection in a monomorphic, ancestral population. Foraging differences between the sexes cannot lead to the evolution of RSD; evolution of large and small morphs of both sexes is a more likely outcome. Selection for sex-role differentiation factors (e.g. large females lay larger eggs, small males are more agile in flight) can lead to the evolution of RSD, but only if the magnitudes of opposing selection for small males and for large females are equal. Combining selection for size-related foraging differences with selection for sex-role differentiation factors hinders the evolution of RSD until the sexes differ in size by 3 s.d . Empirical evidence supports this assertion: statistically significant differences between the sexes in the size of prey taken are found only in highly dimorphic species. The sex-role differentiation factors that have been proposed appear unlikely to provide the equal selection necessary for the evolution of RSD. Several authors have proposed that small size in males is selected for foraging ability and large size in females for some sex-role differentiation factor. Males cannot be more efficient foragers without females being less efficient and efficiency cannot be a factor only when the male is feeding his family. RSD cannot evolve in monogamous species if large females survive less well than small males. RSD might evolve as the result of sexual selection for small size in males and constraints on the reduction of size in females because of some factor associated with reproduction. Examination of seven studies indicating a relationship between female size and reproductive success shows very little unequivocal evidence for small size in females allowing breeding earlier in the season. Large size in females allows females to breed at a younger age in the sparrowhawk and pairs to form more rapidly in three species of sandpipers. Both of these may be the result of sexual selection. There are fewer theoretical problems with sexual selection as a cause for the evolution of RSD than with the other hypotheses. Empirical evidence for sexual selection is scarce but better than that for the other hypotheses. Evidence is contradictory for the selection of small size in males for agility in aerial displays for courtship or defence of territory. Large size in females does not appear to be the result of selection for competitive ability to obtain mates. Facilitation of female dominance and hence of the formation and maintenance of a pair bond is the most viable explanation of the evolution of RSD. It is most likely that all dimorphism (normal or reversed) is the result of sexual selection. RSD is correlated with birds in the diet in the Falconiformes and this is a central theme in the foraging hypotheses. This correlation may be because birds are abundant and available in a continuum of sizes, thus permitting but not causing the evolution of RSD or because species that prey upon birds are better equipped physically (and perhaps more likely behaviourally) to inflict damaging attacks on conspecifics and the greater RSD increases female dominance and the ease of pair formation.     

SEXUAL SELECTION IN THE MONOGAMOUS BARN SWALLOW (HIRUNDO RUSTICA). I. DETERMINANTS OF TAIL ORNAMENT SIZE

The proportion of phenotypic variance in the length of the sexually selected tail of the monogamous barn swallow Hirundo rustica that is attributable to genetic variance was studied in the field in Denmark during a seven-year period. Tail length was on average 20% greater in males than in females. Tail length correlated with wing length, but not with other morphological traits. Tail length increased with the first molt, but remained constant during subsequent years. Changes in tail length between years, owing to molt were significantly affected by sex and by degree of infection with an haematophagous mite (Ornithonyssus bursa). There were significant differences in sexual size dimorphism between years, apparently as a result of environmental conditions in the African winter quarters during molt. Tail length was a highly repeatable morphological trait, and standardization of tail length for age effects only marginally increased repeatability. Heritability of tail length as estimated from regression of values for sons on those of their fathers was 0.59. This suggests that secondary sexual traits affected by strong directional selection still may show a statistically significant heritability.     

INTERACTION-INDEPENDENT SEXUAL SELECTION AND THE MECHANISMS OF SEXUAL SELECTION

Darwin identified explicitly two types of sexual selection, male contests (combat and displays) and female choice, and he devoted the overwhelming majority of his examples to traits that influence the outcome of these interactions. Subsequent treatments of sexual selection have emphasized the importance of intra- and intersexual interactions as sources of sexual selection. However, many traits that are important determinants of mating success influence mating success without necessarily affecting the outcome of intra- and intersexual interactions. Here, I argue that traits can be subject to sexual selection even if they do not affect the outcome of intra- and intersexual interactions. I distinguish two types of sexual selection, interaction-independent and interaction-dependent selection, based on whether variance in mating success is the result of trait-dependent outcomes of interactions between conspecifics. I then use this distinction to construct a framework for classifying types of sexual selection that unifies and expands previously proposed frameworks. Finally, I outline several implications that the concept of interaction-independent sexual selection has for the general theory of sexual selection.     

THE EVOLUTION OF SEXUAL DIMORPHISM BY SEXUAL SELECTION: THE SEPARATE EFFECTS OF INTRASEXUAL SELECTION AND INTERSEXUAL SELECTION

Libellula luctuosa, a pond dragonfly found in eastern North America, is apparently sexually dimorphic. Previous studies of the mating behavior in this species suggested that both male-male competition and female mate choice are important influences. Males compete for territories, where they attract females and where mating occurs. Female behavior influences both the copulation success and the fertilization success of males. Because of temporal and spatial separation of these episodes of sexual selection, multivariate and nonparametric statistical techniques could be used to investigate the influence of components of sexual selection on various sexually dimorphic traits. Sexual dimorphism in L. luctuosa was first quantified; then the direct effects and the form of selection were estimated. Sexually dimorphic wing size, body size, wing coloration, and body coloration are distributed either continuously or discontinuously between the sexes in L. luctuosa. These traits have apparently diverged between the sexes as a result of directional sexual selection. Body size is further influenced by stabilizing selection. Intrasexual selection (success in gaining access to a territory) and intersexual selection (success in copulation and fertilization) can influence the same or different sexually dimorphic characters. Body size is influenced by directional selection during the intrasexual phase of sexual selection and is also influenced by stabilizing selection during intersexual selection. The size of the brown wing patch is influenced by directional selection, primarily during the intersexual phase of sexual selection. There is directional selection on the white wing patch during both phases. Thus, the different proximate mechanisms of sexual selection may jointly or separately affect the evolution of sexually dimorphic characters. Further empirical and theoretical investigations into the differences in the effects of intrasexual selection and intersexual selection are needed to clarify the circumstances leading to separate consequences of these two mechanisms of sexual selection.     

SEXUAL SELECTION AND THE EVOLUTION OF SEXUAL SIZE DIMORPHISM IN THE WATER STRIDER,AQUARIUS REMIGIS

Sexual size dimorphism (SSD) is often attributed to sexual selection, particularly when males are the larger sex. However, sexual selection favoring large males is common even in taxa where females are the larger sex, and is therefore not a sufficient explanation of patterns of SSD. As part of a more extensive study of the evolution of SSD in water striders (Heteroptera, Gerridae), we examine patterns of sexual selection and SSD in 12 populations of Aquarius remigis. We calculate univariate and multivariate selection gradients from samples of mating and single males, for two sexually dimorphic traits (total length and profemoral width) and two sexually monomorphic traits (mesofemoral length and wing form). The multivariate analyses reveal strong selection favoring larger males, in spite of the female-biased SSD for this trait, and weaker selection favoring aptery and reduced mesofemoral length. Selection is weakest on the most dimorphic trait, profemoral width, and is stabilizing rather than directional. The pattern of sexual selection on morphological traits is therefore not concordant with the pattern of SSD. The univariate selection gradients reveal little net selection (direct + indirect) on any of the traits, and suggest that evolution away from the plesiomorphic pattern of SSD is constrained by antagonistic patterns of selection acting on this suite of positively correlated morphological traits. We hypothesize that SSD in A. remigis is not in equilibrium, a hypothesis that is consistent with both theoretical models of the evolution of SSD and our previous studies of allometry for SSD. A negative interpopulation correlation between the intensity of sexual selection and the operational sex ratio supports the hypothesis that, as in several other water strider species, sexual selection in A. remigis occurs through generalized female reluctance rather than active female choice. The implications of this for patterns of sexual selection are discussed.     

ON THE OPPORTUNITY FOR SEXUAL SELECTION, THE BATEMAN GRADIENT AND THE MAXIMUM INTENSITY OF SEXUAL SELECTION

Bateman's classic paper on fly mating systems inspired quantitative study of sexual selection but also resulted in much debate and confusion. Here, I consider the meaning of Bateman's principles in the context of selection theory. Success in precopulatory sexual selection can be quantified as a mating differential, which is the covariance between trait values and relative mating success. The mating differential is converted into a selection differential by the Bateman gradient, which is the least squares regression of relative reproductive success on relative mating success. Hence, a complete understanding of precopulatory sexual selection requires knowledge of two equally important aspects of mating patterns: the mating differential, which requires a focus on mechanisms generating covariance between trait values and mating success, and the Bateman gradient, which requires knowledge of the genetic mating system. An upper limit on the magnitude of the selection differential on any sexually selected trait is given by the product of the standard deviation in relative mating success and the Bateman gradient. This latter view of the maximum selection differential provides a clearer focus on the important aspects of precopulatory sexual selection than other methods and therefore should be an important part of future studies of sexual selection.     

DYNAMICS OF SEXUAL SELECTION IN DIPLOID POPULATIONS

We describe results for a diploid, two-locus model for the evolution of a female mating preference directed at an attractive male trait that is subject to viability and/or fertility selection. Using computer simulation, we studied a large, random sample of parameter values, assuming additivity of alleles at the preference locus and partial dominance at the trait locus. Simulation results were classifiable into nine types of parameter sets, each differing in equilibria, evolutionary trajectories, and rates of evolution. For many parameters, evolutionary trajectories converged on curves within the allelic frequency plane and subsequently evolved along the curves toward fixation. Neutrally stable curves of equilibria did not occur in Fisherian models that assume only viability and sexual selection unless there is complete dominance at the trait locus. The Fisherian models also exhibited oscillation of allelic frequencies and unique polymorphic equilibria. “Sexy son” models in which attractive males had reduced fertility were much less likely to lead to increase in traits and preferences than were the Fisherian models. However, if less fertile males had increased viability, trait polymorphisms and fixation of rare “sexy” alleles occurred. In general, the behavior of the diploid model was much more complex than that of analogous haploid or polygenic models.     

THE ROLE OF MULTILEVEL SELECTION IN THE EVOLUTION OF SEXUAL CONFLICT IN THE WATER STRIDER AQUARIUS REMIGIS

In evolution, exploitative strategies often create a paradox in which the most successful individual strategy “within” the group is also the most detrimental strategy “for” the group, potentially resulting in extinction. With regard to sexual conflict, the overexploitation of females by harmful males can yield similar consequences. Despite these evolutionary implications, little research has addressed why sexual conflict does not ultimately drive populations to extinction. One possibility is that groups experiencing less sexual conflict are more productive than groups with greater conflict. However, most studies of sexual conflict are conducted in a single isolated group, disregarding the potential for selection among groups. We observed Aquarius remigis water striders in a naturalistic multigroup pool in which individuals could freely disperse among groups. The free movement of individuals generated variation in aggression and sex‐ratio among groups, thereby increasing the importance of between‐group selection compared to within‐group selection. Females dispersed away from local aggression, creating more favorable mating environments for less‐aggressive males. Furthermore, the use of contextual analysis revealed that individual male aggression positively predicted fitness whereas aggression at the group level negatively predicted fitness, empirically demonstrating the conflict between levels of selection acting on mating aggression.     

SEASONAL VARIATION IN SEXUAL SELECTION IN THE MOTTLED SCULPIN

Seasonal variation in sexual and natural selection in male mottled sculpins (Cottus bairdi) can be evaluated by calculating selection differentials, which measure the magnitude of phenotypic change resulting from selection, and by calculating indices of the opportunity for selection, which indicate the potential for phenotypic selection in a given interval. Selection differentials are high at the beginning of the breeding season and decline throughout the breeding season. The magnitude and direction of selection differentials depend on when spawning occurs and are independent of the size or age of the females that spawn. Annual selection differentials due to differences in mating success (female choice) are nearly constant between years. Annual selection differentials associated with hatching success are variable. Opportunities for selection (I = fitness variance/[mean fitness]²) show clear seasonal patterns. They are highest at the beginning and at the end of the spawning season. However, this variation is dependent on the mean used to calculate I, and hence variation in I values does not indicate a significant change in the variance of male fitness.     

THE ROLES OF LIFE‐HISTORY SELECTION AND SEXUAL SELECTION IN THE ADAPTIVE EVOLUTION OF MATING BEHAVIOR IN A BEETLE

Although there is continuing debate about whether sexual selection promotes or impedes adaptation to novel environments, the role of mating behavior in such adaptation remains largely unexplored. We investigated the evolution of mating behavior (latency to mating, mating probability and duration) in replicate populations of seed beetles Callosobruchus maculatus subjected to selection on life‐history (“Young” vs. “Old” reproduction) under contrasting regimes of sexual selection (“Monogamy” vs. “Polygamy”). Life‐history selection is predicted to favor delayed mating in “Old” females, but sexual conflict under polygamy can potentially retard adaptive life‐history evolution. We found that life‐history selection yielded the predicted changes in mating behavior, but sexual selection regime had no net effect. In within‐line crosses, populations selected for late reproduction showed equally reduced early‐life mating probability regardless of mating system. In between‐line crosses, however, the effect of life‐history selection on early‐life mating probability was stronger in polygamous lines than in monogamous ones. Thus, although mating system influenced male–female coevolution, removal of sexual selection did not affect the adaptive evolution of mating behavior. Importantly, our study shows that the interaction between sexual selection and life‐history selection can result in either increased or decreased reproductive divergence depending on the ecological context.     

高体鳑鲏的性选择问题研究

以高体鳑鲏为研究对象,分别设置个体大小不同的雌鱼和雄鱼进行性选择实验并验证性选择理论,对雌鱼的怀卵量和雄鱼的空间学习记忆能力也进行了检测。雄鱼对雌鱼的性选择实验结果表明,雄鱼对大个体雌鱼有明显的选择偏好;雄鱼选择雌鱼的次数及停留时间与雌鱼的体长、体高、产卵管长度等特征呈正相关。推测雄鱼是基于直接收益的角度,即最大限度的获得较多的后代及较高的后代存活率对雌鱼进行选择,因为大个体雌鱼拥有长的产卵管及绝对多的处于Ⅴ时相的成熟卵粒,可以提供较多的后代及较高的后代存活率。雌鱼对雄鱼的性选择结果表明,雌性高体鳑鲏对大个体雄鱼也表现出了明显的偏好;雌鱼选择雄鱼的次数及停留时间与雄鱼的体长、体高呈正相关;大个体雄鱼的空间学习记忆能力比小个体强,能更快捷地找到并占领质量好的河蚌而成为领域鱼。从直接收益的观点看,雌鱼选择大个体的雄鱼可能是因为大个体雄鱼可以更加容易、迅速和便捷地寻找到质量好的河蚌引领雌鱼进行产卵,从而保证子代的存活率。