The neurogenetics of sexually dimorphic behaviors from a postdevelopmental perspective

Most sexually reproducing animal species are characterized by two morphologically and behaviorally distinct sexes. The genetic, molecular and cellular processes that produce sexual dimorphisms are phylogenetically diverse, though in most cases they are thought to occur early in development. In some species, however, sexual dimorphisms are manifested after development is complete, suggesting the intriguing hypothesis that sex, more generally, might be considered a continuous trait that is influenced by both developmental and postdevelopmental processes. Here, we explore how biological sex is defined at the genetic, neuronal and behavioral levels, its effects on neuronal development and function, and how it might lead to sexually dimorphic behavioral traits in health and disease. We also propose a unifying framework for understanding neuronal and behavioral sexual dimorphisms in the context of both developmental and postdevelopmental, physiological timescales. Together, these two temporally separate processes might drive sex‐specific neuronal functions in sexually mature adults, particularly as it pertains to behavior in health and disease.     

Influence of incubation temperature on hatchling phenotype in reptiles

Incubation temperature influences hatchling phenotypes such as sex, size, shape, color, behavior, and locomotor performance in many reptiles, and there is growing concern that global warming might adversely affect reptile populations by altering frequencies of hatchling phenotypes. Here I overview a recent theoretical model used to predict hatchling sex of reptiles with temperature-dependent sex determination. This model predicts that sex ratios will be fairly robust to moderate global warming as long as eggs experience substantial daily cyclic fluctuations in incubation temperatures so that embryos are exposed to temperatures that inhibit embryonic development for part of the day. I also review studies that examine the influence of incubation temperature on posthatch locomotion performance and growth because these are the traits that are likely to have the greatest effect on hatchling fitness. The majority of these studies used artificial constant-temperature incubation, but some have addressed fluctuating incubation temperature regimes. Although the number of studies is small, it appears that fluctuating temperatures may enhance hatchling locomotor performance. This finding should not be surprising, given that the majority of natural reptile nests are relatively shallow and therefore experience daily fluctuations in incubation temperature.     

Does gestational temperature or prenatal sex ratio influence development of sexual dimorphism in a viviparous skink?

Prenatal sex ratio (through exposure to hormones from siblings in utero) can influence sexually dimorphic traits of many mammals; but research on viviparous reptiles has contrasting outcomes, which have yet to be resolved. The thermal environment experienced during gestation has a strong effect on the phenotype of reptiles, but whether this thermal effect overrides that of prenatal sex ratio has yet to be explored. We experimentally investigated whether the gestation temperature, or litter sex ratio, influences sexually dimorphic traits (head width and axilla-groin length) in a viviparous skink (Oligosoma maccanni). We found that gestation temperature had a significant influence on sexually dimorphic traits of neonates, and at 3 months of age still influenced head width. We found no evidence that traits in either sex were masculinized or feminized in response to litter sex ratio. The development of external sexual dimorphisms increased gradually (all thermal regimes pooled), with neonates showing no sexual dimorphism, 3-month-old juveniles showing some sexual dimorphism in head width, and adults having stronger, but incompletely separated, sexual dimorphism for both traits. We suggest that the overlap in sexually dimorphic traits of adult O. maccanni (and perhaps other reptiles) may be better explained by natural variation in temperatures experienced during embryonic development, rather than hormonal effects arising from litter sex ratio. The interaction of hormones and temperature during gestation and the effect of these factors on sexual dimorphism within reptiles deserve further exploration.     

Multiple behavioral contexts of a melanized tail display in a desert lizard

Conspicuous color displays in animals are often studied in the context of how they communicate an individual's reproductive value, ability to escape capture, or overall health. The study of sexual dichromatism often focuses on the evolution of male display traits balanced between detectability and mate acquisition, representing constraints stemming from both natural and sexual selection. Melanistic coloration and melanin color patterns play important roles in both intraspecific and interspecific signaling in animals; as melanin serves multiple purposes in organismal biology, the evolution of melanin-based visual displays might not be restricted to a single behavioral or ecological context. Here, we examine the behavioral contexts of the conspicuous melanin-based tail display in the greater earless lizard (Cophosaurus texanus), asking if this melanized tail pattern is associated with (a) female association preference of males varying in the concentration of melanin, (b) individual locomotor performance capacity, and (c) thermal ecology. We found the amount of tail melanin is linked with both locomotor performance and female association preference, with greater concentrations of melanin predicting the evolution of faster performance capacities and females preferring males with more discrete melanin bars. We found limited support that differences in melanin are linked with thermoregulation or thermal ecology. Overall, we find that multiple behavioral contexts shape the evolution of this melanized display trait. We conclude that behavioral constraints stemming from both natural and sexual selection can interact synergistically to favor the evolution and expression of a melanistic visual display, even in potentially costly ecological contexts.     

Sexual differences in locomotor performance in Tropidurus catalanensis lizards (Squamata: Tropiduridae) – body shape,size and limb musculature explain variation between males and females

Sexual dimorphism (SD) is the evolutionary outcome of selection acting differently on males and females. Several studies describe sexual differences in body size, although other morphological traits might be allometric between sexes and imply functional consequences. Here we test whether morphological differences between sexes in size and shape in the lizard Tropidurus catalanensis explain variation in performance of four locomotor traits. Our results show that males are larger than females and also exhibit longer limbs, longer muscles and larger muscle cross‐sectional areas, while females have longer trunks and more sharped anterior claws; males outperform females in all locomotor performances measured. Sexual differences in sprinting and climbing is related with body size, and climbing performance is also explained by limb lengths, by differences in lengths and cross‐sectional areas of specific muscles, and by interlimb distances. Between‐sex differences in exertion are also related to SD, despite associations with sharper posterior claws that are independent of sex. Grasping performance, however, is associated with some muscle and morphological parameters that are not sexually dimorphic. Together our results suggest that morphology might be under sexual selection in T. catalanensis, given that better locomotor performance likely favours male lizards in typical activities of this polygenic species, such as territory defence and female acquisition. Moreover, the longer trunks that characterize females may confer more space to accommodate eggs. On the other hand, territory defence by males probably increases their exposure to predators, resulting in a synergistic effect of sexual and natural selection in the evolution of SD in T. catalanensis.     

Sexual selection and the brain

Sex differences are intrinsically interesting, particularly in the brain. When sexually dimorphic structures mediate learning, and when such learning ability is necessary to compete for mates, then such differences are best understood within the framework of sexual selection. By categorizing recent studies of sex differences in the brain by their role in mate competition, theories of sexual selection can be used to predict and characterize the occurrence of dimorphisms among species with different mating systems.     

Sex and Weapons: Contrasting Sexual Dimorphisms in Weaponry and Aggression in Snapping Shrimp

Sexual dimorphisms in weaponry and aggression are common in species in which one sex (usually males) competes for access to mates or resources necessary for reproduction – sexually dimorphic weaponry and aggression, in other words, are frequently the result of intrasexual selection. In snapping shrimp, the major chela (snapping claw) can be a deadly weapon, and males of many species have larger chelae than females, a pattern readily interpreted as resulting from intrasexual selection. Thus, males might be expected to show more sex‐specific aggression than females, and be more aggressive overall. We tested these predictions in two species of snapping shrimp in a territorial defense context. Neither of these predictions was supported: in both species, females, but not males, engaged in sex‐specific aggression and females were more aggressive than males overall. These contrasting sexual dimorphisms – larger weaponry in males but higher aggression in females – highlight the importance of considering the function of weaponry and aggression in contexts other than direct competitions over mates. In addition, species differences in the degree of sexual dimorphism in chela size were due to differences in female, not male, chela size, and the species with greater sexual dimorphism in weaponry was significantly less aggressive overall; also, while paired and solitary males did not differ in residual chela size, for the species with greater sexual dimorphism, females carrying embryos had smaller residual chela sizes. These results suggest that understanding the sexual dimorphisms in weaponry and aggression in snapping shrimp requires understanding the relative costs and benefits of both in females as well as males.     

Meek Males and Fighting Females: Sexually-Dimorphic Antipredator Behavior and Locomotor Performance Is Explained by Morphology in Bark Scorpions (Centruroides vittatus)

Sexual dimorphism can result from sexual or ecological selective pressures, but the importance of alternative reproductive roles and trait compensation in generating phenotypic differences between the sexes is poorly understood. We evaluated morphological and behavioral sexual dimorphism in striped bark scorpions (Centruroides vittatus). We propose that reproductive roles have driven sexually dimorphic body mass in this species which produces sex differences in locomotor performance. Poor locomotor performance in the females (due to the burden of being gravid) favors compensatory aggression as part of an alternative defensive strategy, while male morphology is coadapted to support a sprinting-based defensive strategy. We tested the effects of sex and morphology on stinging and sprinting performance and characterized overall differences between the sexes in aggressiveness towards simulated threats. Greater body mass was associated with higher sting rates and slower sprinting within sexes, which explained the greater aggression of females (the heavier sex) and, along with longer legs in males, the improved sprint performance in males. These findings suggest females are aggressive to compensate for locomotor costs of reproduction while males possess longer legs to enhance sprinting for predator evasion and mate finding. Sexual dimorphism in the metasoma (“tail”) was unrelated to stinging and sprinting performance and may best be explained by sexual selection.     

Understanding sex differences in the cost of terrestrial locomotion

Little is known regarding the physiological consequences of the behavioural and morphological differences that result from sexual selection in birds. Male and female Svalbard rock ptarmigans (Lagopus muta hyperborea) exhibit distinctive behavioural differences during the breeding season. In particular, males continuously compete for and defend territories in order to breed successfully, placing large demands on their locomotor system. Here, we demonstrate that male birds have improved locomotor performance compared with females, showing both a lower cost of locomotion (CoL) and a higher top speed. We propose that the observed sex differences in locomotor capability may be due to sexual selection for improved male performance. While the mechanisms underlying these energetic differences are unclear, future studies should be wary when pooling male and female data.     

Bending for love: losses and gains of sexual dimorphisms are strictly correlated with changes in the mounting position of sepsid flies (Sepsidae: Diptera)

Background  

Sexually dimorphic structures ntribute the largest number of morphological differences between closely related insect species thus implying that these structures evolve fast and are involved in speciation. The current literature focuses on the selective forces that drive these changes, be it 'sexual conflict' or 'female choice'. However, there are only few studies examining the function of sexual dimorphisms and even fewer that investigate how functional changes influence dimorphisms. This is largely due to the paucity of taxa for which the morphology, behavior, and phylogenetic relationships for multiple species are known. Here we present such data for sepsid flies. Sepsids have starkly dimorphic forelegs whose function can be documented under laboratory conditions. We use data from 10 genes to reconstruct the phylogenetic relationships for 33 species and test whether mounting positions are correlated with the presence and absence of sexual dimorphisms in the forelegs.     

Locomotor performance and social dominance in male Anolis cristatellus

The proximal mechanisms determining social dominance are not well understood. We used the highly territorial lizard A. cristatellus to test two main hypotheses: (1) that male social dominance is associated with locomotor abilities; (2) that locomotor abilities (maximal performance), as measured in the laboratory, are correlated with behaviour in the field. In the field, we recorded locomotor behaviours and assertion displays, then characterized microhabitat use and thermal relations. In the laboratory, we measured maximum sprint running speed, endurance and morphometric characters, and assessed dominance by pairing males of similar body size in an experimental arena. In 72 of 77 interactions, one lizard (the ‘winner’) was unequivocally determined to be dominant over the other (the ‘loser’). Winners performed more assertion displays than losers before capture and also had higher endurance in laboratory tests. Although contestants were matched for snout-vent length, winners had significantly deeper and wider heads. However, we found no significant differences in field locomotor behaviours, perch or thermal characteristics, head length, or maximal sprint speed. Our findings support those of previous studies, and extend them in several ways. This is the first demonstration that assertion displays in the field are related to both locomotor performance and laboratory-assessed social dominance. Locomotor performance may directly affect social dominance by allowing some males to perform better in dyadic interactions. Alternatively, both locomotor performance and social dominance may be linked to a common underlying mechanism, such as variation in hormone levels, which are known to affect aggression, locomotor performance and morphology.     

Sexual dimorphisms in the overall proportions of primates

Morphometric analysis of Professor A.H. Schultz's data on the overall proportions of primates reveals differences between the sexes. Univariate examinations of these data confirm the existence of the spectrum of sexual dimorphism already well known. This spectrum relates mainly to differences in the proportions of the trunk. It has a differential expression with largest differences between the sexes in species such as orangutans and boboons, and smallest in species such as spider monkeys and douroucoulis. Multivariate statistical study of these same data reveal, however, further unsuspected sexual dimorphisms. Although differences between the sexes are only small when measures of the relative lengths of bodily parts are examined, they are big when bodily breadths are studied. Investigation of breadths alone reveals that the primates display two major patterns of sexual dimorphisms and seven unique sexual dimorphisms among the 18 genera examined. Such findings mean that sexual dimorphism of bodily structure is not a single phenomenon with differential expression, a concept widely noted in the literature and most recently associated with social organization. There are several different sexual dimorphisms and this suggests that their causation is likely to be multifactorial with multiple complex interactions among the factors. Some of the sexual dimorphisms must have evolved in parallel a number of times, and, given that chimpanzees, gorillas, and humans each display a different sexual dimorphism, at least some of the evolutionary changes in different sexual dimorphisms must be very recent. The findings even imply the possibility of further unique patterns of sexual dimorphism in some fossils. By further extension, the findings may have some implications for our understanding of nonstructural dimorphisms in humans.     

Phenotypic responses of hatchlings to constant versus fluctuating incubation temperatures in the multi-banded krait, Bungarus multicintus (Elapidae)

Most studies on egg incubation in reptiles have relied on constant temperature incubation in the laboratory rather than on simulations of thermal regimes in natural nests. The thermal effects on embryos in constant-temperature studies often do not realistically reflect what occurs in nature. Recent studies have increasingly recognized the importance of simulating natural nest temperatures rather than applying constant-temperature regimes. We incubated Bungarus multicintus eggs under three constant and one fluctuating-temperature regimes to evaluate the effects of constant versus fluctuating incubation temperatures on hatching success and hatchling phenotypes. Hatching success did not differ among the four treatments, and incubation temperature did not affect the sexual phenotype of hatchlings. Incubation length decreased as incubation temperature increased, but eggs incubated at fluctuating temperatures did not differ from eggs incubated at constant temperatures with approximately the same mean in incubation length. Of the hatchling phenotypes examined, residual yolk, fat bodies and locomotor performance were more likely affected by incubation temperature. The maximal locomotor speed was fastest in the fluctuating-temperature and 30 degrees C treatments and slowest in the 24 degrees C treatment, with the 27 degrees C treatment in between. The maximal locomotor length was longest in the fluctuating-temperature treatment and shortest in the 24 degrees C and 27 degrees C treatments, with the 30 degrees C treatment in between. Our results show that fluctuating incubation temperatures do not influence hatching success and hatchling size and morphology any differently than constant temperatures with approximately the same mean, but have a positive effect on locomotor performance of hatchlings.     

Serum starvation induces sexual dimorphisms in secreted proteins of human umbilical vein endothelial cells (HUVECs) from twin pairs

There is growing evidence for sex and gender differences in the clinical manifestation and outcomes of human diseases. Human primary endothelial cells represent a useful cardiovascular model to study sexual dimorphisms at the cellular level. Here, we analyzed sexual dimorphisms of the secretome after serum starvation using human umbilical vein endothelial cells (HUVECs) from twin pairs of the opposite sex to minimize the impact of varying genetic background. HUVECs were starved for 5 and 16 h, respectively, and proteins of the cell culture supernatants were analyzed by tandem mass spectrometry. Altogether, 960 extracellular proteins were identified of which 683 were amendable to stringent quantification. Significant alterations were observed for 455 proteins between long-term and short-term starvation and the majority were similar in both sexes. Only 5 proteins showed significant sex-specific regulation between long-versus short-term starvation. Furthermore, 19 unique proteins with significant sexual dimorphisms at the same time points of serum starvation were observed. A larger number of proteins, for example tissue factor inhibitor 2 (TFPI2), displayed higher levels in the supernatants of females compared to male cells after long term serum starvation that might point to higher adaptation capacity of female cells. The overall results demonstrate that male and female cells differ in their secretome.     

Functional and ecological correlates of ecologically-based dimorphisms in squamate reptiles

Sexual dimorphism in phenotypic traits associated with the useof resources is a widespread phenomenon throughout the animalkingdom. While ecological dimorphisms are often initially generatedby sexual selection operating on an animal's size, natural selectionis believed to maintain, or even amplify, these dimorphismsin certain ecological settings. The trophic apparatus of snakeshas proven to be a model system for testing the adaptive natureof ecological dimorphisms because head size is rarely undersexual selection and it limits the maximum ingestible size ofprey in these gape-limited predators. Significantly less attentionhas been paid to the evolution of ecological dimorphisms inlizards, however, which may be due to the fact that lizards’feeding apparatus can be under both sexual and natural selectionsimultaneously, making it difficult to formulate clear-cut hypothesesto distinguish between the influences of natural and sexualselection. In order to tease apart the respective influencesof natural selection and sexual selection on the feeding apparatusof squamates, we take an integrative approach to formulate twohypotheses for snakes and lizards, respectively: (1) For gape-limitedsnakes, we predict that natural selection will act to generatedifferences in maximum gape, which will translate into differencesin maximum ingestible prey size between the sexes. (2) For lizardswhich mechanically reduce their prey, we predict that the degreeof dimorphism in head size should be positively correlated tothe degree of dimorphism in bite force which, in turn, shouldbe correlated to dimorphism in aspects of size or hardness ofprey. Finally, we predict that functional differences in thefeeding apparatus of these animals will also be linked withdifferences in sex-based feeding behavior and with selectionof prey.     

When do meadow vipers (Vipera ursinii) become sexually dimorphic? – ontogenetic patterns of sexual size dimorphisms

Contrary to an increasing number of papers that document sexual dimorphism in size (and/or shape) in adults, studies dealing with sex differences in newborn and juvenile snakes are surprisingly scarce. Data about ontogenetic shifts in sexual dimorphism are generally lacking and hence, it is unclear whether sex differences are set at birth or arise post‐natally. In this study, we analyzed patterns of sexual dimorphism in body size, head dimensions and tail length (TL) among newborn, subadult and adult meadow vipers (Vipera ursinii) from the Bjelasica Mt. in Montenegro. Patterns of sexual size dimorphisms differed among traits. There was no significant difference in head dimension of males and females, but adult snakes were sexually dimorphic in body size. Sexual differences in TL were evident since birth but changed in degree throughout ontogeny. Neonate meadow vipers presented highly significant inter‐litter variation in the sexual dimorphism of all traits we have measured. Such family effects may have an important influence on extent of inter‐sexual differences in snakes and should be included in analyses of sexual dimorphism.     

Circadian Rhythms in Amphibians and Reptiles: Ecological Implications

Circadian rhythms of amphibians and reptiles in the field and under semi-natural conditions and the underlying mechanisms, including the ways of entrainment to environmental cues and the oscillators driving the rhythms, have been reviewed. Studies on the behavioral rhythms in the field are meager in both amphibians and reptiles. In anuran amphibians, Xenopus adults showed more robust nocturnal locomotor activity than did tadpoles. This indicates the ecological significance of the differences in activity pattern shown by amphibians at different life stages, because differences between adults and young in the same environment may serve to isolate partially the young from the adults' cannibalism. In reptiles, free-running rhythms are more robust and continue for a longer time compared to amphibians. In both amphibians and reptiles, multi-photoreceptors are involved in photo-entrainment of circadian rhythms. The eyes, pineal complex and deep brain comprise a multi-oscillator system as well as a multi-photoreceptor system.