Sexually size dimorphic brains and song complexity in passerine birds

Neural correlates of bird song involve the volume of particularsong nuclei in the brain that govern song development, production,and perception. Intra- and interspecific variation in the volumeof these song nuclei are associated with overall brain size,suggesting that the integration of complex songs into the brainrequires general neural augmentation. In a comparative studyof passerine birds based on generalized least square models,we tested this hypothesis by exploring the interspecific relationshipbetween overall brain size and repertoire size. We found nosignificant association between song complexity of males andbrain size adjusted for body size. However, species in whichmales produced complex songs tended to have sex differencesin overall brain size. This pattern became stronger when wecontrolled statistically for female song complexity by usingsex differences in song complexity. In species with large differencesin song complexity, females evolved smaller brains than didmales. Our results suggest no role for the evolution of extendedneural space, as reflected by total brain size, owing to songcomplexity. However, factors associated with sexual selectionmirrored by sex differences in song complexity were relatedto sexual dimorphism in overall brain size.     

Sperm size and sperm competition in birds.

In a sample of 20 species of North American passerine birds we found no relation between sperm size and mating system like that previously reported in mammals (Gomendio & Roldan (Proc. R. Soc. Lond. B 243, 181 (1991)). Instead, we found a positive correlation between sperm length and the length of female sperm storage tubules (SSTS) and a negative correlation between sperm length and the number of SSTS. Both of these correlations suggest that the more than fivefold variation in sperm size we found among species can be explained by sperm competition for access to storage sites (SSTS) in females. As longer sperm appear to be able to swim faster, selection should favour long sperm when SSTS are in short supply; sperm long enough to fill an SST might also prevent access to SSTS by the sperm of other males. Conversely, selection should favour shorter sperm when there is an advantage to sperm layering within an SST promoting a last-male mating advantage. Although we conclude that sperm competition influences sperm size in birds, little is known about the interactions between sperm and SSTS. It seems clear, however, that detailed study of this interaction will provide a new dimension to the study of avian mating systems.     

Sperm competition and the evolution of testes size in birds

Comparative analyses suggest that a variety of ecological and behavioural factors contribute to the tremendous variability in extrapair mating among birds. In an analysis of 1010 species of birds, we examined several ecological and behavioural factors in relation to testes size; an index of sperm competition and the extent of extrapair mating. In univariate and multivariate analyses, testes size was significantly larger in species that breed colonially than in species that breed solitarily, suggesting that higher breeding density is associated with greater sperm competition. After controlling for phylogenetic effects and other ecological variables, testes size was also larger in taxa that did not participate in feeding their offspring. In analyses of both the raw species data and phylogenetically independent contrasts, monogamous taxa had smaller testes than taxa with multiple social mates, and testes size tended to increase with clutch size, which suggests that sperm depletion may play a role in the evolution of testes size. Our results suggest that traditional ecological and behavioural variables, such as social mating system, breeding density and male parental care can account for a significant portion of the variation in sperm competition in birds.     

Sperm competition in birds

Ornithologists have known for a long time that males of monogamous bird species sometimes copulate with females from other pairs, but it is only in the last few years that researchers have shown that these extra-pair copulations can result in offspring and increase male reproductive success. Males time their extra-pair copulations to coincide with the period when females are fertilizable, and they show a range of remarkable behaviours to help them secure these matings, since in most cases females attempt to avoid them. At the same time, males of most species employ one of two strategies (mate guarding or frequent copulation) to avoid being cuckolded themselves.     

Sperm competition and sperm midpiece size: no consistent pattern in passerine birds

Sperm competition is thought to be a major force driving the evolution of sperm shape and function. However, previous studies investigating the relationship between the risk of sperm competition and sperm morphometry revealed inconclusive results and marked differences between taxonomic groups. In a comparative study of two families of passerines (Fringillidae and Sylviidae) and also across species belonging to different passerine families, we investigated the relative importance of the phylogenetic background on the relationship between sperm morphometry and the risk of sperm competition. The risk of sperm competition was inferred from relative testis mass as an indicator of investment in sperm production. We found: (i) a significant positive association between both midpiece length and flagellum length and relative testis mass in the Fringillidae, (ii) a significant negative association between sperm trait dimensions and relative testis mass in the Sylviidae, and (iii) no association across all species. Despite the striking difference in the patterns shown by the Sylviidae and the Fringillidae, the relationship between midpiece length and flagellum length was positive in both families and across all species with positive allometry. Reasons for the differences and similarities between passerine families are discussed.     

Sperm competition games played by dimorphic male beetles

Reproductive strategies often consist of two alternative tactics whereby males either compete for and guard females, or sneak copulations. By their nature, alternative tactics expose males to differing risks of sperm competition; sneaks will always be subject to sperm competition but guards will be subject to sperm competition with low probability, dependent on the number of sneaks. Recent game-theoretical models predict that males in the sneak role should have the greater gametic expenditure but that the disparity in expenditure should decrease with increasing numbers of sneaks. Male dung beetles in the genus Onthophagus can be separated into two morphs: major males have horns and guard females whereas minor males are hornless and sneak copulations. Here we compare testis size and ejaculate characteristics between these alternative morphs. We find that in O. binodis 30% of males are sneaks, and sneaks have larger testes, ejaculate volumes, and longer sperm than guards. In O. taurus 60% of males are sneaks and there are no differences in gametic traits. Our data thus provide empirical support for game-theoretical models of sperm competition.     

Sperm competition in tropical versus temperate zone birds

Sperm competition represents an important component of post-copulatory sexual selection. It has been argued that the level of sperm competition declines in birds towards the equator. However, to date, sperm competition estimates have been available mainly for avian species inhabiting the northern temperate zone. Here we apply a novel approach, using the coefficient of between-male variation (CV_bm) in sperm size as an index for sperm competition risk, in a comparative analysis of 31 Afrotropical and 99 northern temperate zone passerine species. We found no difference in sperm competition risk between the two groups, nor any relationship with migration distance. However, a multivariate model indicated that sperm competition risk was highest in species with a combination of low body mass and few eggs per clutch. The effect of clutch size was most pronounced in tropical species, which indicates that sperm competition risk in tropical and temperate species is differently associated with particular life-history traits. Although tropical species had lower sperm competition risk than temperate zone species for overlapping clutch sizes, the idea of a generally reduced risk of sperm competition in tropical birds was not supported by our analysis.     

Sperm competition mechanisms in birds: models and data

This study presents three models to explain the mechanism oflast male sperm precedence in birds. Because passive loss ofsperm from the female reproductive tract occurs, all modelsincorporate this process. The three models are passive spermloss alone, stratification with passive sperm loss, and displacementwith passive sperm loss. With two inseminations containing thesame number of sperm, the models make the following predictions.For passive sperm loss alone, (1) differential paternity ispositively and linearly related to the time interval betweeninseminations, (2) with a slope that is equal to rate of lossof sperm from the female reproductive tract, (3) with an interceptthat is the same as the differential fertilizing capacity betweenthe semen of the two inseminations, and (4) the ratio of offspringfrom two inseminations remains constant over time. For stratification,(1) the relationship between differential paternity and theinterval between inseminations is nonlinear and exhibits a "brokenstick" pattern, with a substantial first-insemination precedencefor short intervals, and (2) the proportion of offspring fatheredby the first insemination increases over time. For displacement,the relationship between differential paternity and the intervalbetween inseminations is nonlinear and also exhibits a "brokenstick" pattern, but in contrast to the stratification model,sperm from the last insemination have precedence. Data fromthree experimental studies of the domestic fowl and one forthe turkey provide the opportunity to test these models, albeitto different extents. The data from all studies are consistentwith the passive sperm-loss model, except that one aspect ofone data set provided ambiguous support for stratification.None of the data provided any support for the displacement model.     

Sperm competition and brain size evolution in mammals

The ‘expensive tissue hypothesis’ predicts a size trade‐off between the brain and other energetically costly organs. A specific version of this hypothesis, the ‘expensive sexual tissue hypothesis’, argues that selection for larger testes under sperm competition constrains brain size evolution. We show here that there is no general evolutionary trade‐off between brain and testis mass in mammals. The predicted negative relationship between these traits is not found for rodents, ungulates, primates, carnivores, or across combined mammalian orders, and neither does total brain mass vary according to the level of sperm competition as determined by mating system classifications. Although we are able to confirm previous reports of a negative relationship between brain and testis mass in echolocating bats, our results suggest that mating system may be a better predictor of brain size in this group. We conclude that the expensive sexual tissue hypothesis accounts for little or none of the variance in brain size in mammals, and suggest that a broader framework is required to understand the costs of brain size evolution and how these are met.     

First evidence of sex differences in the duration of avian embryonic period: consequences for sibling competition in sexually dimorphic birds

Parental favoritism in birds would be enhanced if parents cancontrol any egg feature influencing the ontogeny of the embryoduring incubation. Egg size and composition may influence theduration of incubation and hatching periods, and eggs bearingembryos of different sex may differ in size and composition.Therefore, the sex of the embryo could also influence its ontogenybefore hatching. We tested this prediction by investigatingthe duration of the embryonic period of different-sex embryosin the Eurasian kestrel (Falco tinnunculus), a sexually dimorphicraptor in which adult females are approximately 20% heavierthan are adult males. We found the first evidence of sex differencesin the duration of the embryonic period in avian eggs. Femaleembryos had a shorter embryonic period than did male embryos,which allowed females to hatch earlier in the hatching sequenceand assume a higher rank than that of males in the intrabroodsize hierarchy. Embryos with a fast growth and development resultedin hatchlings with greater residual reserves and thus largermass, which suggests that a shorter embryonic period requiresless maintenance metabolism relative to growth. Our resultsalso indicated that early hatching may be advantageous to gaina high rank in the size hierarchy within the brood independentlyof the effect of sex on fledgling mass. Sex differences in avianegg ontogeny may therefore be a factor shaping life-historytraits associated with parental control of sibling competition,which should be addressed in any future work on optimal reproductiveinvestment.     

Sperm competition influences sperm size in mammals.

Among mammals sperm competition leads to selection for increased sperm numbers but it is not known whether it also leads to changes in sperm size. Two contrasting theoretical predictions have been made. The first hypothesis relies on the assumption that there is a trade-off between sperm numbers and sperm size and predicts that, in species confronting sperm competition, there will be a concomitant decrease in sperm size as sperm numbers increase. In contrast, the second hypothesis suggests that longer sperm may outcompete rival sperm; if longer sperm may swim faster, they will reach the ova sooner and will be selected when sperm competition prevails. We tested these hypotheses in both primates and rodents. We report that males from species in which females mate promiscuously have longer sperm than species in which females mate with one male. In addition, we also found that sperm length is positively correlated with maximum sperm velocity. Our findings thus support the view that longer sperm may be adaptive in the context of sperm competition.     

Testes size, ejaculate quality and sperm competition in birds

The relationship between testes size, ejaculate quality (volume, sperm concentration, number of sperm per ejaculate) and sperm competition in birds was analysed using data collected in artificial insemination studies. I hypothesized that ejaculate quality, because of natural selection, should be superior in species with intense sperm competition compared with other species. In regression analyses, testes weight increased with body weight, with an exponent less than one, and ejaculate volume increased with testes weight with an exponent not significantly different from one, whereas sperm number per ejaculate increased with testes weight with an exponent larger than one. Species with relatively large testes also produced ejaculates with a high sperm concentration. Monogamous species with a relatively low intensity of sperm competition copulate rarely, but deliver ejaculates with a relatively large number of sperm. Monogamous species with a high intensity of sperm competition copulate frequently, but produce ejaculates with a relatively small number of sperm. Males of polygynous species, which also experience intense sperm competition, copulate rarely with specific females, but produce many ejaculates per male each with a relatively small number of sperm.     

Sperm size of African cichlids in relation to sperm competition

We compared pairs of closely related taxa of cichlid fishesfrom Lake Tanganyika to examine the relationship between spermsize and the presumed intensity of sperm competition. In contrastto previous reports of relatively short sperm in polygamousfishes across a variety of taxa, we found that polygamous cichlidshad significantly longer sperm than their closest monogamousrelatives. In addition, sperm length was significantly relatedto relative testis size (controlling for body size and phylogeny).The site of fertilization may also be correlated with spermlength, as species that fertilize in the female's buccal cavityhad significantly shorter sperm than those that fertilizedeggs on the substrate. Assuming that relatively large testesand polygamous mating are indicative of more intense sperm competition, these results indicate that sperm length is related to the intensityof sperm competition in this clade of cichlids, as has beenfound previously in insects, birds, and mammals.     

The allometric pattern of sexually size dimorphic feather ornaments and factors affecting allometry

The static allometry of secondary sexual characters is currently subject to debate. While some studies suggest an almost universal positive allometry for such traits, but isometry or negative allometry for nonornamental traits, other studies maintain that any kind of allometric pattern is possible. Therefore, we investigated the allometry of sexually size dimorphic feather ornaments in 67 species of birds. We also studied the allometry of female feathers homologous to male ornaments (female ornaments in the following) and ordinary nonsexual traits. Allometries were estimated as reduced major axis slopes of trait length on tarsus length. Ornamental feathers showed positive allometric slopes in both sexes, although that was not a peculiarity for ornamental feathers, because nonsexual tail feathers also showed positive allometry. Migration distance (in males) and relative size of the tail ornament (in females) tended to be negatively related to the allometric slope of tail feather ornaments, although these results were not conclusive. Finally, we found an association between mating system and allometry of tail feather ornaments, with species with more intense sexual selection showing a smaller degree of allometry of tail ornaments. This study is consistent with theoretical models that predict no specific kind of allometric pattern for sexual and nonsexual characters.     

Sperm competition games between sneaks and guards: a comparative analysis using dimorphic male beetles

Sperm competition is widely recognized as a pervasive force of sexual selection. Theory predicts that across species increased risk of sperm competition should favor an increased expenditure on the ejaculate, a prediction for which there is much evidence. Sperm competition games have also been developed specifically for systems in which males adopt the alternative male mating tactics of sneaking copulations or guarding females. These models have not yet been tested in a comparative context, but predict that: across species male expenditure on the ejaculate should increase with increasing probability of a sneak mating; within species, sneaks should have the greater expenditure on the ejaculate; and the disparity in expenditure between sneaks and guards should be greatest in species with moderate risk of a sneak mating, and decline toward parity in species with low or high risk. Beetles in the genus Onthophagus are often characterized by dimorphic male morphologies that reflect the alternative mating tactics of sneak (minor males) and guard (major males). We conducted a comparative analysis across 16 species of male dimorphic onthophagines, finding that testes size increased across species with increasing frequency of the minor male phenotype. Minor males generally had the greater testes size, but across species the disparity between morphs was independent of the frequency of minor males. We present data on testes allometry from two populations of O. taurus that have undergone genetic divergence in the frequency of minor males. Consistent with the comparative analysis, these data support the notion that the relative frequency of sneaks in the population influences male expenditure on the ejaculate.     

The relationship between male head size and harem size in the sexually dimorphic mountain stone weta Hemideina maori

Abstract 1. Tree weta are a group of large, flightless orthopterans with pronounced sexual dimorphism. Males have enlarged heads that are used in fighting for possession of cavities in trees or under rocks where females shelter during the day.
2. The fieldwork reported here examined the relationship between male head size and mating success in Hemideina maori , an alpine tree weta that shelters under rock slabs that have broken off isolated outcrops or tors.
3. The relationship between male head size and harem size in H. maori is not as clear-cut as thought previously. First, overall body size is a better predictor of male mating success than head size per se . Second, both body size and head size explained a relatively low percentage (19.8%) of the overall variation in mating success. Third, despite the intensity of directional selection being estimated to move the frequency distribution of head size and femur size 0.49 and 0.54 standard deviations from the mean, male heads and femurs were ≈ 2 mm smaller at the main study site than at a second site 100 m higher in elevation. A similar pattern was found for adult females. Additional surveys have indicated that body size in H. maori decreases with decreasing altitude, which is correlated with increasing night-time temperature.
4. Although there are reasons why natural selection might favour weta maturing earlier and at smaller body sizes in warmer environments, relatively large males would still have a mating advantage over smaller males under such conditions. This sexually dimorphic alpine insect might be a good example of the trade-offs and conflicting demands that sexual selection versus natural selection can place on organisms.     

Opposing selection on a sexually dimorphic trait through female choice and male competition in a water boatman

Female choice and male-male competition are traditionally considered to act in concert, with male competition facilitating female choice. This situation would enforce the strength of directional selection, which could reduce genetic variation and thus the benefits of choice. Here I show that in a water boatman, Sigara falleni, the direction of selection through female choice and male competition vary among traits under laboratory conditions. The two forces were mutually enforcive in acting on body size but exerted opposing selection on a sexually selected trait, male foreleg pala size. Female choice favored large palae, whereas male competition favored smaller palae, suggesting that large palae are costly in competition. This conflicting selection through female choice and male competition could be one of the forces that contribute to the maintenance of genetic variation in sexually selected traits.