The evolution of sexual size dimorphism in the house finch. II. Population divergence in relation to local selection

Recent colonization of ecologically distinct areas in North America by the house finch (Carpodacus mexicanus) was accompanied by strong population divergence in sexual size dimorphism. Here we examined whether this divergence was produced by population differences in local selection pressures acting on each sex. In a long-term study of recently established populations in Alabama, Michigan, and Montana, we examined three selection episodes for each sex: selection for pairing success, overwinter survival, and within-season fecundity. Populations varied in intensity of these selection episodes, the contribution of each episode to the net selection, and in the targets of selection. Direction and intensity of selection strongly differed between sexes, and different selection episodes often favored opposite changes in morphological traits. In each population, current net selection for sexual dimorphism was highly concordant with observed sexual dimorphism--in each population, selection for dimorphism was the strongest on the most dimorphic traits. Strong directional selection on sexually dimorphic traits, and similar intensities of selection in both sexes, suggest that in each of the recently established populations, both males and females are far from their local fitness optimum, and that sexual dimorphism has arisen from adaptive responses in both sexes. Population differences in patterns of selection on dimorphism, combined with both low levels of ontogenetic integration in heritable sexually dimorphic traits and sexual dimorphism in growth patterns, may account for the close correspondence between dimorphism in selection and observed dimorphism in morphology across house finch populations.     

The evolution of sexual size dimorphism in the house finch. IV. Population divergence in ontogeny

Differences among taxa in sexual size dimorphism of adults can be produced by changes in distinct developmental processes and thus may reflect different evolutionary histories. Here we examine whether divergence in sexual dimorphism of adults between recently established Montana and Alabama populations of the house finch (Carpodacus mexicanus) can be attributed to population differences in growth of males and females. In both populations, males and females were similar at hatching, but as a result of sex-specific growth attained sexual size dimorphism by the time of independence. Timing and extent of growth varied between the sexes: Females maintained maximum rates of growth for a longer time than males, whereas males had higher initial growth rates and achieved maximum growth earlier and at smaller sizes than females. Ontogeny of sexual dimorphism differed between populations, but in each population, sexual dimorphism in growth parameters and sexual dimorphism at the time of nest leaving were similar to sexual dimorphism of adults. Variation in growth of females contributed more to population divergence than did growth of males. In each population, we found close correspondence between patterns of sexual dimorphism in growth and population divergence in morphology of adults: Traits that were the most sexually dimorphic in growth in each population contributed the most to population divergence in both sexes. We suggest that sex-specific expression of phenotypic and genetic variation throughout the ontogeny of house finches can result in different responses to selection between males and females of the same age, and thus produce fast population divergence in the sexual size dimorphism.     

The evolution of sexual size dimorphism in the house finch. III. Developmental basis

Sexual size dimorphism of adults proximately results from a combination of sexually dimorphic growth patterns and selection on growing individuals. Yet, most studies of the evolution of dimorphism have focused on correlates of only adult morphologies. Here we examined the ontogeny of sexual size dimorphism in an isolated population of the house finch (Carpodacus mexicanus). Sexes differed in growth rates and growth duration; in most traits, females grew faster than males, but males grew for a longer period. Sexual dimorphism in bill traits (bill length, width, depth) and in body traits (wing, tarsus, and tail length; mass) developed during different periods of ontogeny. Growth of bill traits was most different between sexes during the juvenile period (after leaving the nest), whereas growth of body traits was most sexually dimorphic during the first few days after hatching. Postgrowth selection on juveniles strongly influenced sexual dimorphism in all traits; in some traits, this selection canceled or reversed dimorphism patterns produced by growth differences between sexes. The net result was that adult sexual dimorphism, to a large degree, was an outcome of selection for survival during juvenile stages. We suggest that previously documented fast and extensive divergence of house finch populations in sexual size dimorphism may be partially produced by distinct environmental conditions during growth in these populations.     

Sexual dimorphism in lizard body shape: the roles of sexual selection and fecundity selection

Sexual dimorphism is widespread in lizards, with the most consistently dimorphic traits being head size (males have larger heads) and trunk length (the distance between the front and hind legs is greater in females). These dimorphisms have generally been interpreted as follows: (1) large heads in males evolve through male-male rivalry (sexual selection); and (2) larger interlimb lengths in females provide space for more eggs (fecundity selection). In an Australian lizard (the snow skink, Niveoscincus microlepidotus), we found no evidence for ongoing selection on head size. Trunk length, however, was under positive fecundity selection in females and under negative sexual selection in males. Thus, fecundity selection and sexual selection work in concert to drive the evolution of sexual dimorphism in trunk length in snow skinks.     

Condition-dependent sexual traits and social dominance in the house finch

Elaboration of costly sexual traits can reduce investment inother aspects of reproduction, such as parental care or intrasexualcompetition, which may lead to the evolution of alternativemating tactics. In house finches (Carpodacus mexicanus), lesselaborately ornamented (dull) males tend to dominate more elaborated(redder) males, but redder males pair earlier and invest morein parental care. This suggests that males may pursue alternativeparental or competitive tactics, depending on the elaborationof their sexual trait. Elevation of testosterone, a hormonethat is closely associated with condition in male house finches,influences dominance and sexual behaviors but is antagonisticto parental behaviors. We tested the hypothesis that the higherdominance status of dull males reflects an alternative testosterone-dependentmating tactic. First, we experimentally manipulated the testosteronelevels of captive males and measured the effect on dominancerank, and second, we measured the association of testosteroneelevation and plumage hue in free-living males. We found that,as predicted, testosterone elevation increased dominance rankin captive males. However, in free-living males, testosteronelevels were higher in redder males, suggesting that testosteroneis dissociated from dominance status under natural circumstances.This may be because the context of social interactions and thehigher motivation of dull males to access food resources havea stronger influence on the outcome of dominance interactionsthan does the physiological effects of testosterone elevation.In turn, the strong positive correlation between testosteronelevels and plumage elaboration likely reflects the common conditiondependence of these traits.     

Sexual selection and sexual size dimorphism in animals

Sexual selection is often considered as a critical evolutionary force promoting sexual size dimorphism (SSD) in animals. However, empirical evidence for a positive relationship between sexual selection on males and male-biased SSD received mixed support depending on the studied taxonomic group and on the method used to quantify sexual selection. Here, we present a meta-analytic approach accounting for phylogenetic non-independence to test how standardized metrics of the opportunity and strength of pre-copulatory sexual selection relate to SSD across a broad range of animal taxa comprising up to 95 effect sizes from 59 species. We found that SSD based on length measurements was correlated with the sex difference in the opportunity for sexual selection but showed a weak and statistically non-significant relationship with the sex difference in the Bateman gradient. These findings suggest that pre-copulatory sexual selection plays a limited role for the evolution of SSD in a broad phylogenetic context.     

Sexual dimorphism in weight among the primates: The relative impact of allometry and sexual selection

In this paper, we examine allometric and sexual-selection explanations for interspecific differences in the amount of sexual dimorphism among 60 primate species. Based on evidence provided by statistical analyses, we reject Leutenegger and Cheverud’s [(1982). Int. J. Primatol.3:387-402] claim that body size alone is the major factor in the evolution of sexual dimorphism. The alternative proposed here is that sexual selection due to differences in the reproductive potential of males and females is the primary cause of sexual dimorphism. In addition, we propose that the overall size of a species determines whether the dimorphism will be expressed as size dimorphism,rather than in some other form.     

Sexual size dimorphism in the great tit (Parus major) in relation to history and current selection

We investigated the possible causes of the evolution of sexual size and shape dimorphism in the great tit (Parus major) by using two different approaches. First, we used the equilibrium approach, i.e. analysing current selection to see whether it was possible to find directional selection in the direction of the dimorphism, or stabilising selection maintaining dimorphism at its current level. Second, we used the historical approach, i.e. putting the degree of dimorphism in a phylogenetic perspective to analyse what kind of changes (if any) have occurred. This was carried out in the following way: (i) we described the level of sexual dimorphism in a population of Swedish great tits by means of path model. (ii) We used the path model design to analyse survival and reproductive selection in this population. (iii) We compared the level of dimorphism in relation to size in the great tit with that of the closest congener, the blue tit P. caeruleus. (iv) We compared the amount of interspecific morphological variation with that which would be expected under a drift model. We found no evidence of either stabilising or directional survival or reproductive selection. Size and shape variation in the great tit seemed unrelated to fitness in adults. Dimorphism was somewhat greater in the great tit compared to the blue tit, but only with an amount predictable by its larger size. In terms of phenotypic standard deviations, the great tit was not more dimorphic than the blue tit, although it was larger. The amount of interspecific variance with regard to size was lower or equal to that expected by the drift model, showing that long-term directional selection for an increase in size and dimorphism is improbable. These results agree with recent theoretical findings that size and dimorphism should be related and that strong conservatism with regard to dimorphism is to be expected. They also agree with the view that in equilibrium populations, fitness components (if there are many of them) should appear neutral with regard to total fitness.     

嘉陵江下游蛇鮈的两性异形与雌性个体生殖力

为了解蛇鮈雌雄间是否存在显著的外部形态差异及雌性个体生殖力情况, 在繁殖期对嘉陵江下游(合川江段)共76尾蛇鮈样本的两性异形、性比及雌性个体生殖力进行分析.结果表明: 嘉陵江下游蛇鮈繁殖群体的性比接近1∶1,且蛇鮈两性的体型大小相同,但局部特征(如头部和躯干部等)呈现出显著的两性异形,如成体雄性蛇鮈的头部、胸鳍和腹鳍均较雌性蛇鮈大,而躯干部的体宽、体高和躯干长则是雌性蛇鮈大于雄性蛇鮈,这可能是性选择长期作用的结果.主成分分析显示,前3个主成分的累积贡献率达75.2%,但雌雄个体间形态特征相互重叠,无法将两者截然分开;利用判别函数对蛇鮈性别进行回判,综合判别准确率为92.1%.蛇鮈雌性个体绝对生殖力在979～19979粒;且与体长和去内脏体质量均呈显著正相关.同历史资料相比,本研究中嘉陵江蛇鮈的生殖力增大显著,这可能是蛇鮈对种群资源量下降和水环境变化主动适应的结果.     

The evolution of sexual dimorphism in the house finch. I. Population divergence in morphological covariance structure

Abstract Patterns of genetic variation and covariation strongly affect the rate and direction of evolutionary change by limiting the amount and form of genetic variation available to natural selection. We studied evolution of morphological variance-covariance structure among seven populations of house finches (Carpodacus mexicanus) with a known phylogenetic history. We examined the relationship between within- and among-population covariance structure and, in particular, tested the concordance between hierarchical changes in morphological variance-covariance structure and phylogenetic history of this species. We found that among-population morphological divergence in either males or females did not follow the within-population covariance patterns. Hierarchical patterns of similarity in morphological covariance matrices were not congruent with a priori defined historical pattern of population divergence. Both of these results point to the lack of proportionality in morphological covariance structure of finch populations, suggesting that random drift alone is unlikely to account for observed divergence. Furthermore, drift alone cannot explain the sex differences in within- and among-population covariance patterns or sex-specific patterns of evolution of covariance structure. Our results suggest that extensive among-population variation in sexual dimorphism in morphological covariance structure was produced by population differences in local selection pressures acting on each sex.     

Sexual dimorphism in growth from 8 to 18 years

A mixed longitudinal study of growth and development has been conducted, centering on an analysis of differences based on sex between the ages of 8 and 18 years for a series of 12 anthropometric indicators. The sample consisted of 50 girls and 63 boys. Proceeding from the specific differences, the variables can be divided into four groups with identical structures of differences. The first group comprises measurements of body height, body mass, shoulder width and pelvic span, all of which have higher values in boys between 8 and 10 and between 14 and 18. Between the ages of 11 and 13 girls are taller, heavier, with broader shoulders and pelvises. The second group covers measurements of subcutaneous fat. which are higher for girls throughout the period under review. The third group of indicators comprises the diameters of the joints of the extremities, i.e. of elbows and knees. Throughout the period under observation, these measurements are higher in boys, with the absolute differences between the sexes being the same at the age of 8 and ten years later. The fourth group consists of circumferences measurements of the extremities. It was found that calf circumferences manifested a specific inversion of the curves between 14 and 15, with girls showing a larger calf circumference up to the age of 14, and boys from the age of 15. The effect of earlier onset of puberty in girls was found to be reflected only on the inversion of the curve flow of the variables from the first group.     

Sexual size dimorphism and reproductive ecology in relation to mating system in waders

The relationship between sexual size dimorphism, body-weight and different reproductive traits (e.g. clutch size, egg weight and incubation period) in relation to mating system and forms of parental care was studied in waders. Two hypotheses were examined. (1) Sexual size dimorphism is correlated with the intensity of sexual selection. (2) The degree of sexual size dimorphism is the result of an interrelationship between the reproductive strategy of the female and her body size. In the polygynous species the male was significantly larger than the female. This is consistent with the sexual selection hypothesis. However, among waders, a positive correlation exists between egg weight, clutch mass and body-weight. Selection for small eggs or a short incubation period may therefore have an influence on female body-weight. If the lack of paternal care reduces the female's possibility for producing large eggs or incubating a large clutch mass, we would expect a selection pressure for small female size among polygynous species. Thus, large sexual size dimorphism among polygynous waders may be a result of selection for small female size to lack of paternal care, or selection for large male size due to intramale competition or a female preference for large-sized males. In multiple-clutch species (viz. species in which the female regularly lays more than one clutch during the season) egg weight was low both for a given female and male body-weight. The low egg weight of multiple-clutch species is assumed to be a result of the constraints placed on the female from producing several clutches during a single breeding season.     

Sexual selection, sexual size dimorphism and Rensch's rule in Odonata

Odonata (dragonflies and damselflies) exhibit a range of sexual size dimorphism (SSD) that includes species with male-biased (males > females) or female-biased SSD (males < females) and species exhibiting nonterritorial or territorial mating strategies. Here, we use phylogenetic comparative analyses to investigate the influence of sexual selection on SSD in both suborders: dragonflies (Anisoptera) and damselflies (Zygoptera). First, we show that damselflies have male-biased SSD, and exhibit an allometric relationship between body size and SSD, that is consistent with Rensch's rule. Second, SSD of dragonflies is not different from unit, and this suborder does not exhibit Rensch's rule. Third, we test the influence of sexual selection on SSD using proxy variables of territorial mating strategy and male agility. Using generalized least squares to account for phylogenetic relationships between species, we show that male-biased SSD increases with territoriality in damselflies, but not in dragonflies. Finally, we show that nonagile territorial odonates exhibit male-biased SSD, whereas male agility is not related to SSD in nonterritorial odonates. These results suggest that sexual selection acting on male sizes influences SSD in Odonata. Taken together, our results, along with avian studies (bustards and shorebirds), suggest that male agility influences SSD, although this influence is modulated by territorial mating strategy and thus the likely advantage of being large. Other evolutionary processes, such as fecundity selection and viability selection, however, need further investigation.     

Sexual dimorphism in relation to swarming and pair formation patterns in leptocerid caddisflies (Trichoptera: Leptoceridae)

North European Leptoceridae (Trichoptera) perform three types of swarming flight patterns: (1) swarming males of Athripsodesand Ceracleafly in horizontal zigzag patterns over the water surface, (2) the Mystacidesspp. perform vertical zigzag movements, and (3) the flight of males of Triaenodes unanimisMcLach. is a mixture of the horizontal and vertical zigzagging. Also three groups of pair formation behavior can be distinguished. In the first group, of Athripsodesand Ceraclea,the females fly into the male swarms, where they are grasped and carried to the riparian vegetation by the flying males with the females hanging upside-down in genitalia coupling. In the second group, a Mystacidesfemale is caught by a male, when approaching a swarm and both use their wings to fly in tandem to the shore where they copulate. In the third group, of Triaenodes bicolor(Curt.) and Oecetis lacustris(Curt.), the males fly searching for females sitting on aquatic plants and when a female is found the male lands and they copulate immediately while clinging to the plant. The different swarming and mating behaviors might have favored selection for three types of sexual dimorphism: (1) longer forewings in males than females in species which fly in copula, (2) larger eyes in males of the vertically zigzagging species, and (3) much smaller males in the group where males search for females sitting on aquatic plants. In the second group approaching females are detected by males before reaching the swarm and in the third group the female almost always mates with the male which is the first to find her. In conclusion, we suggest that females of Athripsodesand Ceracleahave a greater choice among swarming males than do females of Mystacides, T. bicolor,and O. Lacustris.     

Sexual size dimorphism and selection in the wild in the waterstrider Aquarius remigis: Body size,components of body size and male mating success

Sexual size dimorphism is assumed to be adaptive and is expected to evolve in response to a difference in the net selection pressures on the sexes. Although a demonstration of sexual selection is neither necessary nor sufficient to explain the evolution of sexual size dimorphism, sexual selection is generally assumed to be a major evolutionary force. If contemporary sexual selection is important in the evolution and maintenance of sexual size dimorphism then we expect to see concordance between patterns of sexual selection and patterns of sexual dimorphism. We examined sexual selection in the wild, acting on male body size, and components of body size, in the waterstrider Aquarius remigis, as part of a long term study examining net selection pressures on the two sexes in this species. Selection was estimated on both a daily and annual basis. Since our measure of fitness (mating success) was behavioral, we estimated reliabilities to determine if males perform consistently. Reliabilities were measured as ? statistics and range from fair to perfect agreement with substantial agreement overall. We found significant univariate sexual selection favoring larger total length in the first year of our study but not in the second. Multivariate analysis of components of body size revealed that sexual selection for larger males was not acting directly on total length but on genital length. Sexual selection for larger male body size was opposed by direct selection favoring smaller midfemoral lengths. While males of this species are smaller than females, they have longer genital segments and wider forefemora. Patterns of contemporary sexual selection and sexual size dimorphism agree only for genital length. For total length, and all other components of body size examined, contemporary sexual selection was either nonsignificant or opposed the pattern of size dimporhism. Thus, while the net pressures of contemporary selection for the species may still act to maintain sexual size dimorphism, sexual selection alone does not.     

Sexual size dimorphism,prey morphology and catch success in relation to flight mechanics in the peregrine falcon: a simulation study

In common with many other raptors, female peregrine falcons Falco peregrinus are about 50% heavier than males. Their sexual dimorphism is thought to allow breeding pairs to exploit a wider range of prey through a division of labor: the male being able to catch more maneuverable prey species; the female capable of carrying larger ones. Given the difficulty of assessing the catch success and load carrying capacity of both sexes of falcon in the field, we here adopt a novel approach to test the division‐of‐labor theory by using a detailed physics‐based flight simulator of birds. We study attacks by male and female peregrines on prey species ranging from small passerines to large ducks, testing how catch success relates to the flight performance of predator and prey. Males prove to be better than females at catching highly maneuverable prey in level flight, but the catch success of both sexes improves and becomes more similar when diving, because of the higher aerodynamic forces that are available to both sexes for maneuvering in high‐speed flight. The higher maximum roll acceleration of the male peregrine explains its edge over the female in catching maneuverable prey in level flight. Overall, catch success is more strongly influenced by the differences in maneuverability that exist between different species of prey than between the different sexes of falcon. On the other hand, the female can carry up to 50% greater loads than the male. More generally, our detailed simulation approach highlights the importance of several previously overlooked features of attack and escape. In particular, we find that it is not the prey's instantaneous maximum centripetal acceleration but the prey's ability to sustain a high centripetal acceleration for an extended period of time that is the primary driver of the variation in catch success across species.     

Muscle‐dependent and hormone‐dependent differentiation of the vocal control premotor nucleus robustus archistriatalis and the motornucleus hypoglossus pars tracheosyringealis of the zebra finch

Sex differences in the vertebrate brain (brain sex) are thought to develop owing to the tissue specific action of gonadal hormones similar to the development of secundary sex characteristics of the body. Small sex differences in body anatomy could, however, retrogradely control the sexual differentiation of the central nervous system. This possibility has so far been verified only for motorneuron pools, since the connectivity of sex‐specific higher brain areas to the sexual dimorphic periphery is frequently not well known. Here, we tested whether somatic sex differences feed back on higher brain areas by bilateral denervation of the syringeal musculature of zebra finches before, during, and after onset of estrogen‐sensitive sexual differentiation of forebrain vocal nuclei such as RA (nucleus robustus archistriatalis). In the zebra finch, the sound‐producing musculature (the syrinx), the syrinx motornucleus hypolossus pars tracheosyringealis (nXIIts), and the RA are much larger in males compared to females. Tract tracing studies revealed that the volume and neuron size distribution of the nXIIts was sexually dimorphic in intact but not in animals denervated as juveniles. In contrast, the volume of RA and size of RA neurons of denervated animals were highly sexually dimorphic. Furthermore, estrogen masculinized the RA of denervated females. Thus, sexual differentiation of the RA but not of the nXIIts appears independent of somatic sex differences. The syrinx muscles are, however, important for the soma size of those RA neurons that project to the nXIIts. © 2000 John Wiley & Sons, Inc. J Neurobiol 42: 220–231, 2000     

Sexual selection on male size drives the evolution of male‐biased sexual size dimorphism via the prolongation of male development

Sexual size dimorphism (SSD) arises when the net effects of natural and sexual selection on body size differ between the sexes. Quantitative SSD variation between taxa is common, but directional intraspecific SSD reversals are rare. We combined micro‐ and macroevolutionary approaches to study geographic SSD variation in closely related black scavenger flies. Common garden experiments revealed stark intra‐ and interspecific variation: Sepsis biflexuosa is monomorphic across the Holarctic, while S. cynipsea (only in Europe) consistently exhibits female‐biased SSD. Interestingly, S. neocynipsea displays contrasting SSD in Europe (females larger) and North America (males larger), a pattern opposite to the geographic reversal in SSD of S. punctum documented in a previous study. In accordance with the differential equilibrium model for the evolution of SSD, the intensity of sexual selection on male size varied between continents (weaker in Europe), whereas fecundity selection on female body size did not. Subsequent comparative analyses of 49 taxa documented at least six independent origins of male‐biased SSD in Sepsidae, which is likely caused by sexual selection on male size and mediated by bimaturism. Therefore, reversals in SSD and the associated changes in larval development might be much more common and rapid and less constrained than currently assumed.