Extreme Sexual Brain Size Dimorphism in Sticklebacks: A Consequence of the Cognitive Challenges of Sex and Parenting?

Selection pressures that act differently on males and females produce numerous differences between the sexes in morphology and behaviour. However, apart from the controversial report that males have slightly heavier brains than females in humans, evidence for substantial sexual dimorphism in brain size is scarce. This apparent sexual uniformity is surprising given that sexually distinct selection pressures are ubiquitous and that brains are one of the most plastic vertebrate organs. Here we demonstrate the highest level of sexual brain size dimorphism ever reported in any vertebrate: male three-spined stickleback of two morphs in an Icelandic lake have 23% heavier brains than females. We suggest that this dramatic sexual size dimorphism is generated by the many cognitively demanding challenges that males are faced in this species, such as an elaborate courtship display, the construction of an ornate nest and a male-only parental care system. However, we consider also alternative explanations for smaller brains in females, such as life-history trade-offs. Our demonstration of unprecedented levels of sexual dimorphism in brain size in the three-spined stickleback implies that behavioural and life-history differences among the sexes can have strong effects also on neural development and proposes new fields of research for understanding brain evolution.     

Song and the song control pathway in the brain can develop independently of exposure to song in the sedge warbler

Previous studies have shown that female sedge warblers choose to mate with males that have more complex songs, and sexual selection has driven the evolution of both song complexity and the size of the major song control area (HVc) in the brain. In songbirds, learning from conspecifics plays a major role in song development and this study investigates the effects of isolation and exposure to song on song structure and the underlying song control system. Sibling pairs of hand-reared nestling sedge warblers were reared to sexual maturity under two conditions. Siblings in one group were reared individually in acoustic isolation in separate soundproof chambers. In the other group, siblings were reared together in an aviary with playback of recorded songs. The following spring, analysis of songs revealed that siblings reared in acoustic isolation produced normal song structures, including larger syllable repertoires than those exposed to song. We found no significant differences in the volumes of HVc, nucleus robustus archistnatalis, the lateral portion of the magnocellular nucleus and the density of dendritic spines between the two groups. Males exceeded females in all these measures, and also had a larger telencephalon. Our experiments show that complex song, sexual dimorphism in brain structure, and the size of song nuclei can all develop independently of exposure to song. These findings have important implications for how sexual selection can operate upon a complex male trait such as song and how it may also shape the more general evolution of brain structure in songbirds.     

Sexual selection predicts brain structure in dragon lizards

Phenotypic traits such as ornaments and armaments are generally shaped by sexual selection, which often favours larger and more elaborate males compared to females. But can sexual selection also influence the brain? Previous studies in vertebrates report contradictory results with no consistent pattern between variation in brain structure and the strength of sexual selection. We hypothesize that sexual selection will act in a consistent way on two vertebrate brain regions that directly regulate sexual behaviour: the medial preoptic nucleus (MPON) and the ventromedial hypothalamic nucleus (VMN). The MPON regulates male reproductive behaviour whereas the VMN regulates female reproductive behaviour and is also involved in male aggression. To test our hypothesis, we used high‐resolution magnetic resonance imaging combined with traditional histology of brains in 14 dragon lizard species of the genus Ctenophorus that vary in the strength of precopulatory sexual selection. Males belonging to species that experience greater sexual selection had a larger MPON and a smaller VMN. Conversely, females did not show any patterns of variation in these brain regions. As the volumes of both these regions also correlated with brain volume (BV) in our models, we tested whether they show the same pattern of evolution in response to changes in BV and found that the do. Therefore, we show that the primary brain nuclei underlying reproductive behaviour in vertebrates can evolve in a mosaic fashion, differently between males and females, likely in response to sexual selection, and that these same regions are simultaneously evolving in concert in relation to overall brain size.     

Sexual segregation in childhood: a review of evidence for two hypotheses

In this paper, I review the evidence associated with two hypotheses, both ultimately derived from sexual selection theory, put forth to explain social sexual segregation in human juveniles. More proximately, I posit that segregation is motivated by sex differences in body size, physical activity and competitiveness. The first hypothesis, the energetic/behavioural hypothesis, suggests that difference in energetics is a way in which males differentiate themselves from females and develop muscle and brain systems implicated in reproductive roles. The second hypothesis, the social roles hypothesis, suggests that segregation is related to learning male and female reproductive roles. The reviewed evidence supports the view that there are differences in energetics in male and female groups. With development, the vigorous behaviours shown by males take the form of specific social roles, related to dominance and competitiveness for males and maternal roles for females.     

Sexual selection and the evolution of male and female cognition: A test using experimental evolution in seed beetles*

The mating system is thought to be important in shaping animal intelligence and sexual selection has been depicted as a driver of cognitive evolution, either directly by promoting superior cognitive ability during mate competition, or indirectly via genic capture of sexually selected traits. However, it remains unclear if intensified sexual selection leads to general improvements in cognitive abilities. Here, we evaluated this hypothesis by applying experimental evolution in seed beetles. Replicate lines, maintained for 35 generations of either enforced monogamy (eliminating sexual selection) or polygamy, were challenged to locate and discriminate among mates (male assays) or host seeds (female assays) in a spatial chemosensory learning task. All lines displayed learning between trials. Moreover, polygamous males outperformed monogamous males, providing evidence that sexual selection can lead to the evolution of improved male cognition. However, there were no differences between regimes in rates of male learning, and polygamous females showed no improvement in host search and even signs of reduced learning. Hence, sexual selection increased performance in cognitively demanding mate search, but it did not lead to general increases in cognitive abilities. We discuss the possibility that sexually antagonistic selection is an important factor maintaining abundant genetic variation in cognitive traits.     

Sexual selection on brain size in shorebirds (Charadriiformes)

Natural selection is considered a major force shaping brain size evolution in vertebrates, whereas the influence of sexual selection remains controversial. On one hand, sexual selection could promote brain enlargement by enhancing cognitive skills needed to compete for mates. On the other hand, sexual selection could favour brain size reduction due to trade‐offs between investing in brain tissue and in sexually selected traits. These opposed predictions are mirrored in contradictory relationships between sexual selection proxies and brain size relative to body size. Here, we report a phylogenetic comparative analysis that highlights potential flaws in interpreting relative brain size‐mating system associations as effects of sexual selection on brain size in shorebirds (Charadriiformes), a taxonomic group with an outstanding diversity in breeding systems. Considering many ecological effects, relative brain size was not significantly correlated with testis size. In polyandrous species, however, relative brain sizes of males and females were smaller than in monogamous species, and females had smaller brain size than males. Although these findings are consistent with sexual selection reducing brain size, they could also be due to females deserting parental care, which is a common feature of polyandrous species. Furthermore, our analyses suggested that body size evolved faster than brain size, and thus the evolution of body size may be confounding the effect of the mating system on relative brain size. The brain size‐mating system association in shorebirds is thus not only due to sexual selection on brain size but rather, to body size evolution and other multiple simultaneous effects.     

Sexual selection uncouples the evolution of brain and body size in pinnipeds

The size of the vertebrate brain is shaped by a variety of selective forces. Although larger brains (correcting for body size) are thought to confer fitness advantages, energetic limitations of this costly organ may lead to trade-offs, for example as recently suggested between sexual traits and neural tissue. Here, we examine the patterns of selection on male and female brain size in pinnipeds, a group where the strength of sexual selection differs markedly among species and between the sexes. Relative brain size was negatively associated with the intensity of sexual selection in males but not females. However, analyses of the rates of body and brain size evolution showed that this apparent trade-off between sexual selection and brain mass is driven by selection for increasing body mass rather than by an actual reduction in male brain size. Our results suggest that sexual selection has important effects on the allometric relationships of neural development.     

ENVIRONMENTAL AND GENETIC CONTROL OF BRAIN AND SONG STRUCTURE IN THE ZEBRA FINCH

Birdsong is a classic example of a learned trait with cultural inheritance, with selection acting on trait expression. To understand how song responds to selection, it is vital to determine the extent to which variation in song learning and neuroanatomy is attributable to genetic variation, environmental conditions, or their interactions. Using a partial cross fostering design with an experimental stressor, we quantified the heritability of song structure and key brain nuclei in the song control system of the zebra finch and the genotype‐by‐environment (G × E) interactions. Neuroanatomy and song structure both showed low levels of heritability and are unlikely to be under selection as indicators of genetic quality. HVC, in particular, was almost entirely under environmental control. G × E interaction was important for brain development and may provide a mechanism by which additive genetic variation is maintained, which in turn may promote sexual selection through female choice. Our study suggests that selection may act on the genes determining vocal learning, rather than directly on the underlying neuroanatomy, and emphasizes the fundamental importance of environmental conditions for vocal learning and neural development in songbirds.     

Sperm competition and sexually size dimorphic brains in birds

Natural selection may favour sexually similar brain size owing to similar selection pressures in males and females, while sexual selection may lead to sexually dimorphic brains. For example, sperm competition involves clear-cut sex differences in behaviour, as males display, mate guard and copulate with females, while females choose among males, and solicit or reject copulations. These behaviours may require fundamentally different neural government in the two sexes leading to sex-dependent brain evolution. Using two phylogenetic approaches in a comparative study, we tested for roles of both natural and sexual-selection pressures on brain size evolution of birds. In accordance with the natural-selection theory, relative brain size of males coevolved with that of females, which may be the result of adaptation to similar environmental constraints such as feeding innovation. However, the mode of brain size evolution differed between the sexes, and factors associated with sperm competition as reflected by extra-pair paternity may give rise to sexually size dimorphic brains. Specifically, species in which females have larger brains than males were found to have a higher degree of extra-pair paternity independently of potentially confounding factors, whereas species in which males have relatively larger brains than females appeared to have lower rates of extra-pair paternity. Hence, the evolution of sperm competition may select for complex behaviours together with the associated neural substrates in the sex that has a higher potential to control extra-pair copulations at the observed levels. Brain function may thus be affected differently in males and females by sexual selection.     

Developmental plasticity in neural circuits controlling birdsong: Sexual differentiation and the neural basis of learning

In many species of passerine songbirds, males learn their song during defined periods of life. Female song in often reduced or absent, as are the brain regions controlling song. Sexual differences in the brain arise because of the action of sex steroids, which trigger the formation of some neural pathways (especially the pathway from the higher vocal center to the robust nucleus) and prevent the atrophy of others in males. These neural changes occur during periods of developmental song learning and can recur during periods of learning in adult birds. The process of learning is correlated with major increases or decreases in the number of neurons in specific neuronal populations, suggesting that the formation or loss of specific neural pathways regulates the ability to learn. Species differences in sexual differentiation and learning allow informative cross-species comparisons of neural structure and behavior. © 1992 John Wiley & Sons, Inc.     

Causes of male sexual trait divergence in introduced populations of guppies

Males from different populations of the same species often differ in their sexually selected traits. Variation in sexually selected traits can be attributed to sexual selection if phenotypic divergence matches the direction of sexual selection gradients among populations. However, phenotypic divergence of sexually selected traits may also be influenced by other factors, such as natural selection and genetic constraints. Here, we document differences in male sexual traits among six introduced Australian populations of guppies and untangle the forces driving divergence in these sexually selected traits. Using an experimental approach, we found that male size, area of orange coloration, number of sperm per ejaculate and linear sexual selection gradients for male traits differed among populations. Within populations, a large mismatch between the direction of selection and male traits suggests that constraints may be important in preventing male traits from evolving in the direction of selection. Among populations, however, variation in sexual selection explained more than half of the differences in trait variation, suggesting that, despite within‐population constraints, sexual selection has contributed to population divergence of male traits. Differences in sexual traits were also associated with predation risk and neutral genetic distance. Our study highlights the importance of sexual selection in trait divergence in introduced populations, despite the presence of constraining factors such as predation risk and evolutionary history.     

Developmental plasticity in neural circuits controlling birdsong: sexual differentiation and the neural basis of learning.

In many species of passerine songbirds, males learn their song during defined periods of life. Female song is often reduced or absent, as are the brain regions controlling song. Sexual differences in the brain arise because of the action of sex steroids, which trigger the formation of some neural pathways (especially the pathway from the higher vocal center to the robust nucleus) and prevent the atrophy of others in males. These neural changes occur during periods of developmental song learning and can recur during periods of learning in adult birds. The process of learning is correlated with major increases or decreases in the numbers of neurons in specific neuronal populations, suggesting that the formation or loss of specific neural pathways regulates the ability to learn. Species differences in sexual differentiation and learning allow informative cross-species comparisons of neural structure and behavior.     

Sexual selection without sexual dimorphism: Bateman gradients in a simultaneous hermaphrodite

One of the most general patterns in sexual selection is stronger selection on mating activity in males than in females. This asymmetry is thought to result from the higher energetic cost of producing one female compared to one male gamete (anisogamy). However, most studies focused on gonochoric species with strong sexual dimorphism, in which males and females are necessarily under different selection regimes. The question remains whether anisogamy alone would suffice to produce such differences. In simultaneous hermaphrodites one can compare sexual selection on the male and female functions in the absence of sexual dimorphism. Here we quantify sexual selection in the hermaphroditic freshwater snail Physa acuta under laboratory conditions. We combine exhaustive behavioral records of mating activity in mating groups and molecular paternity assignment to measure the mating success and reproductive success of 120 individuals. Our results validate the prediction of stronger selection to gain mating partners in the male than in the female function. Moreover, we did not detect cross‐sex effects on fitness, or correlations between male and female production of offspring over the course of our experiment. We conclude that with respect to sexual selection P. acuta is comparable to gonochorists, confirming that anisogamy is a sufficient explanation for the differences in sexual selection regimes between sexes.     

The impact of learning on sexual selection and speciation

Learning is widespread in nature, occurring in most animal taxa and in several different ecological contexts and, thus, might play a key role in evolutionary processes. Here, we review the accumulating empirical evidence for the involvement of learning in mate choice and the consequences for sexual selection and reproductive isolation. We distinguish two broad categories: learned mate preferences and learned traits under mate selection (such as bird song). We point out that the context of learning, namely how and when learning takes place, often makes a crucial difference to the predicted evolutionary outcome. Factors causing biases in learning and when one should expect the evolution of learning itself are also explored.     

Brain size evolution in pipefishes and seahorses: the role of feeding ecology,life history and sexual selection

Brain size varies greatly at all taxonomic levels. Feeding ecology, life history and sexual selection have been proposed as key components in generating contemporary diversity in brain size across vertebrates. Analyses of brain size evolution have, however, been limited to lineages where males predominantly compete for mating and females choose mates. Here, we present the first original data set of brain sizes in pipefishes and seahorses (Syngnathidae) a group in which intense female mating competition occurs in many species. After controlling for the effect of shared ancestry and overall body size, brain size was positively correlated with relative snout length. Moreover, we found that females, on average, had 4.3% heavier brains than males and that polyandrous species demonstrated more pronounced (11.7%) female‐biased brain size dimorphism. Our results suggest that adaptations for feeding on mobile prey items and sexual selection in females are important factors in brain size evolution of pipefishes and seahorses. Most importantly, our study supports the idea that sexual selection plays a major role in brain size evolution, regardless of on which sex sexual selection acts stronger.     

Evolutionary inevitability of sexual antagonism

Sexual antagonism, whereby mutations are favourable in one sex and disfavourable in the other, is common in natural populations, yet the root causes of sexual antagonism are rarely considered in evolutionary theories of adaptation. Here, we explore the evolutionary consequences of sex-differential selection and genotype-by-sex interactions for adaptation in species with separate sexes. We show that sexual antagonism emerges naturally from sex differences in the direction of selection on phenotypes expressed by both sexes or from sex-by-genotype interactions affecting the expression of such phenotypes. Moreover, modest sex differences in selection or genotype-by-sex effects profoundly influence the long-term evolutionary trajectories of populations with separate sexes, as these conditions trigger the evolution of strong sexual antagonism as a by-product of adaptively driven evolutionary change. The theory demonstrates that sexual antagonism is an inescapable by-product of adaptation in species with separate sexes, whether or not selection favours evolutionary divergence between males and females.     

Sexual selection and tail streamers in the barn swallow

The functional significance of elongated, narrow tips of the tail feathers of certain birds, so-called tail streamers, has recently been discussed from an aerodynamic point of view, and the effects of sexual selection on such traits have been questioned. We review our long-term field studies using observational and experimental approaches to investigate natural and sexual selection in the barn swallow, Hirundo rustica, which has sexually size-dimorphic outermost tail feathers. Experimental manipulation of the length of the outermost tail feathers has demonstrated sexual selection advantages of tail elongation and disadvantages of tail shortening, with opposite effects for natural selection in terms of foraging efficiency, haematocrit and survival. These findings are contrary to the prediction of a general deterioration from both shortening and elongation, if the tail trait was determined solely by its effects on aerodynamic efficiency and flight manoeuvrability. Patterns of sexual selection in manipulated birds conform with patterns in unmanipulated birds, and selection differentials for different components of sexual selection in manipulated birds are strongly positively correlated with differentials in unmanipulated birds. Age and sex differences in tail length, and geographical patterns of sexual size dimorphism, are also consistent with sexual selection theory, but inconsistent with a purely natural selection advantage of long outermost tail feathers in male barn swallows.     

Sexual differences in morphology and niche utilization in an aquatic snake,Acrochordus arafurae

Filesnakes (Acrochordus arafurae) are large (to 2 m), heavy-bodied snakes of tropical Australia. Sexual dimorphism is evident in adult body sizes, weight/length ratios, and body proportions (relative head and tail lengths). Dimorphism is present even in neonates. Two hypotheses for the evolution of such dimorphism are (1) sexual selection or (2) adaptation of the sexes to different ecological niches. The hypothesis of sexual selection is consistent with general trends of sexually dimorphic body sizes in snakes, and accurately predicts, for A. arafurae, that the larger sex (female) is the one in which reproductive success increases most strongly with increasing body size. However, the sexual dimorphism in relative head sizes is not explicable by sexual selection.The hypothesis of adaptation to sex-specific niches predicts differences in habitats and/or prey. I observed major differences between male and female A. arafurae in prey types, prey sizes and habitat utilization (shallow versus deep water). Hence, the sexual dimorphism in relative head sizes is attributed to ecological causes rather than sexual selection. Nonetheless, competition between the sexes need not be invoked as the selective advantage of this character divergence. It is more parsimonious to interpret these differences as independent adaptations of each sex to increase foraging success, given pre-existing sexually-selected differences in size, habitat or behavior. Data for three other aquatic snake species, from phylogenetically distant taxa, suggest that sexual dimorphism in food habits, foraging sites and feeding morphology, is widespread in snakes.     

Localizing Brain Regions Associated with Female Mate Preference Behavior in a Swordtail

Female mate choice behavior is a critical component of sexual selection, yet identifying the neural basis of this behavior is largely unresolved. Previous studies have implicated sensory processing and hypothalamic brain regions during female mate choice and there is a conserved network of brain regions (Social Behavior Network, SBN) that underlies sexual behaviors. However, we are only beginning to understand the role this network has in pre-copulatory female mate choice. Using in situ hybridization, we identify brain regions associated with mate preference in female Xiphophorus nigrensis, a swordtail species with a female choice mating system. We measure gene expression in 10 brain regions (linked to sexual behavior, reward, sensory integration or other processes) and find significant correlations between female preference behavior and gene expression in two telencephalic areas associated with reward, learning and multi-sensory processing (medial and lateral zones of the dorsal telencephalon) as well as an SBN region traditionally associated with sexual response (preoptic area). Network analysis shows that these brain regions may also be important in mate preference and that correlated patterns of neuroserpin expression between regions co-vary with differential compositions of the mate choice environment. Our results expand the emerging network for female preference from one that focused on sensory processing and midbrain sexual response centers to a more complex coordination involving forebrain areas that integrate primary sensory processing and reward.