Changes in Electroencephalogram Approximate Entropy Reflect Auditory Processing and Functional Complexity in Frogs

Brain systems engage in what are generally considered to be among the most complex forms of information processing. In the present study, we investigated the functional complexity of anuran auditory processing using the approximate entropy(Ap En) protocol for electroencephalogram(EEG) recordings from the forebrain and midbrain while male and female music frogs(Babina daunchina) listened to acoustic stimuli whose biological significance varied. The stimuli used were synthesized white noise(reflecting a novel signal), conspecific male advertisement calls with either high or low sexual attractiveness(reflecting sexual selection) and silence(reflecting a baseline). The results showed that 1) Ap En evoked by conspecific calls exceeded Ap En evoked by synthesized white noise in the left mesencephalon indicating this structure plays a critical role in processing acoustic signals with biological significance; 2) Ap En in the mesencephalon was significantly higher than for the telencephalon, consistent with the fact that the anuran midbrain contains a large well-organized auditory nucleus(torus semicircularis) while the forebrain does not; 3) for females Ap En in the mesencephalon was significantly different than that of males, suggesting that males and females process biological stimuli related to mate choice differently.     

Mating Signals Indicating Sexual Receptiveness Induce Unique Spatio-Temporal EEG Theta Patterns in an Anuran Species

Female mate choice is of importance for individual fitness as well as a determining factor in genetic diversity and speciation. Nevertheless relatively little is known about how females process information acquired from males during mate selection. In the Emei music frog, Babina daunchina, males normally call from hidden burrows and females in the reproductive stage prefer male calls produced from inside burrows compared with ones from outside burrows. The present study evaluated changes in electroencephalogram (EEG) power output in four frequency bands induced by male courtship vocalizations on both sides of the telencephalon and mesencephalon in females. The results show that (1) both the values of left hemispheric theta relative power and global lateralization in the theta band are modulated by the sexual attractiveness of the acoustic stimulus in the reproductive stage, suggesting the theta oscillation is closely correlated with processing information associated with mate choice; (2) mean relative power in the beta band is significantly greater in the mesencephalon than the left telencephalon, regardless of reproductive status or the biological significance of signals, indicating it is associated with processing acoustic features and (3) relative power in the delta and alpha bands are not affected by reproductive status or acoustic stimuli. The results imply that EEG power in the theta and beta bands reflect different information processing mechanisms related to vocal recognition and auditory perception in anurans.     

Behavior and Approximate Entropy of Right-eye Lateralization During Predation in the Music Frog

Brain asymmetry for processing visual information is widespread in animals. However, it is still unknown how the complexity of the underlying neural network activities represents this asymmetrical pattern in the brain. In the present study, we investigated this complexity using the approximate entropy(ApEn)protocol for electroencephalogram(EEG) recordings from the forebrain and midbrain while the music frogs(Nidirana daunchina) attacked prey stimulus. The results showed that(1) more significant prey responses were evoked by the prey stimulus presented in the right visual field than that in the left visual field,consistent with the idea that right-eye preferences for predatory behaviors exist in animals including anurans;(2) in general, the ApEn value of the left hemisphere(especially the left mesencephalon) was greatest under various stimulus conditions, suggesting that visual lateralization could be reflected by the dynamics of underlying neural network activities and that the stable left-hemisphere dominance of EEG ApEn may play an important role in maintaining this brain asymmetry.     

Electroencephalographic signals synchronize with behaviors and are sexually dimorphic during the light–dark cycle in reproductive frogs

Male frogs behave differently from females during the breeding season, particularly with respect to courtship displays and in response to mating signals. In search of physiological correlates of these differences, the present study measured changes in baseline electroencephalogram (EEG) power output within four frequency bands in the telencephalon and mesencephalon, together with changes in locomotor activity as a function of the light–dark cycle in male and female Emei music frogs (Babina daunchina) at the reproductive stage. Previous studies have shown that male vocal activity varies both seasonally and daily in this species and that females use male advertisement calls to locate and select mates. The present results show that both EEG and locomotor activity exhibit highly correlated circadian patterns with peaks around light onset and offset. Importantly, during the reproductive stage, statistically significant sex differences in EEG output across brain regions during the light and dark phases were found indicating that sexual dimorphism exists for EEG activity which may underlie sexually specific information processing and behavioral activities.     

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.     

HOMAGE TO BATEMAN: SEX ROLES PREDICT SEX DIFFERENCES IN SEXUAL SELECTION

Classic sex role theory predicts that sexual selection should be stronger in males in taxa showing conventional sex roles and stronger in females in role reversed mating systems. To test this very central prediction and to assess the utility of different measures of sexual selection, we estimated sexual selection in both sexes in four seed beetle species with divergent sex roles using a novel experimental design. We found that sexual selection was sizeable in females and the strength of sexual selection was similar in females and males in role‐reversed species. Sexual selection was overall significantly stronger in males than in females and residual selection formed a substantial component of net selection in both sexes. Furthermore, sexual selection in females was stronger in role‐reversed species compared to species with conventional sex roles. Variance‐based measures of sexual selection (the Bateman gradient and selection opportunities) were better predictors of sexual dimorphism in reproductive behavior and morphology across species compared to trait‐based measures (selection differentials). Our results highlight the importance of using assays that incorporate components of fitness manifested after mating. We suggest that the Bateman gradient is generally the most informative measure of the strength of sexual selection in comparisons across sexes and/or species.     

Behavioral and morphological asymmetries in chukar Alectoris chukar copulation

Birds often exhibit greater reproductive tract development on the left side than right side. Behavioral evidence from the three species for which data has been published indicates that these species copulate more frequently on the left side of females than on the right side. Missing from the literature are studies that compare asymmetry in copulation behavior to asymmetry in reproductive tract morphology of the same individuals of both sexes within a single species. To better understand the potential for cryptic sexual selection to influence avian copulation, we measured asymmetries in chukar Alectoris chukar copulation using 24 male and 29 female chukar brought into captivity from the wild. Chukar copulated (n=37) more from the left side (n=30) of females than the right side (n=7). The left testis of males was consistently greater in size, mass and volume than the right testis. The left ovary and oviduct of females was consistently functional with no observable development of the right ovary or oviduct. Left-side bias in direction of copulation, larger left testes, and functional left vaginal openings may act in concert to deliver spermatozoa to the oviduct, promoting fertilization.     

Spatial and temporal patterns of nest distribution influence sexual selection in a marine fish

In many species, the natural distribution of material resources important for reproduction can profoundly impact reproductive success among individuals and, hence, the opportunity and intensity of sexual selection. Here, we report on a field‐based experiment investigating the effects of nest aggregation on sexual selection in a fish, the sand goby Pomatoschistus minutus. We found that the distribution of potential nests (sparse versus aggregated nest treatments) affected patterns of nest colonization and reproductive success. Specifically, in the treatment with aggregated nesting resources, a greater proportion of nests remained unoccupied by sand goby males. Although the size of nesting males did not differ between treatments, eggs accumulated more rapidly when nests were sparsely distributed. We found that the opportunity for selection decreased over time with the accumulation of eggs in the nests in both the aggregated and sparse treatments. Moreover, the effect of male size on reproductive success was influenced by an interaction between nest distribution and time, with the selection gradient being highest right after nest colonization when nests were aggregated, while the opposite pattern was observed in the sparse nest treatment. Such findings highlight the vital role that environmental and social factors can play in determining the importance of male phenotypic traits (in this case, male size). More broadly, our results also underscore how the natural distribution of resources, both in space and time, can impact the strength of sexual selection acting on wild animal populations.     

Reproductive isolation caused by visual predation on migrants between divergent environments

In theory, natural selection can drive adaptation within species while simultaneously promoting the formation of new species by causing the evolution of reproductive isolation. Cryptic coloration is widespread in nature and is generally considered to be a clear visual example of adaptation. I provide evidence that population divergence in cryptic coloration can also cause reproductive isolation. First, a manipulative field experiment using walking-stick insects demonstrates that the relative survival of different colour-pattern morphs depends on the host-plant species on which they are resting, but only in the presence of avian predation. Second, natural populations adapted to different host plants have diverged in colour-pattern-morph frequencies such that between-host migrants are more likely to be the locally less-cryptic morph than are residents. Collectively, these data indicate that high rates of visual predation on less-cryptic migrants are likely to reduce encounters, and thus interbreeding, between host-associated populations. Comparison with previous estimates of sexual isolation reveals that the contribution of selection against between-host migrants to total premating isolation is as strong as, or stronger than, that of sexual isolation. These findings highlight the potential role of natural selection against migrants between divergent environments in the formation of new species.     

Operational sex ratio, sexual conflict and the intensity of sexual selection

Modern sexual selection theory indicates that reproductive costs rather than the operational sex ratio predict the intensity of sexual selection. We investigated sexual selection in the polygynandrous common lizard Lacerta vivipara . This species shows male aggression, causing high mating costs for females when adult sex ratios (ASR) are male-biased. We manipulated ASR in 12 experimental populations and quantified the intensity of sexual selection based on the relationship between reproductive success and body size. In sharp contrast to classical sexual selection theory predictions, positive directional sexual selection on male size was stronger and positive directional selection on female size weaker in female-biased populations than in male-biased populations. Thus, consistent with modern theory, directional sexual selection on male size was weaker in populations with higher female mating costs. This suggests that the costs of breeding, but not the operational sex ratio, correctly predicted the strength of sexual selection.     

The accumulation of reproductive isolation in early stages of divergence supports a role for sexual selection

Models of speciation by sexual selection propose that male–female coevolution leads to the rapid evolution of behavioural reproductive isolation. Here, we compare the strength of behavioural isolation to ecological isolation, gametic incompatibility and hybrid inviability in a group of dichromatic stream fishes. In addition, we examine whether any of these individual barriers, or a combined measure of total isolation, is predicted by body shape differences, male colour differences, environmental differences or genetic distance. Behavioural isolation reaches the highest values of any barrier and is significantly greater than ecological isolation. No individual reproductive barrier is associated with any of the predictor variables. However, marginally significant relationships between male colour and body shape differences with ecological and behavioural isolation are discussed. Differences in male colour and body shape predict total reproductive isolation between species; hierarchical partitioning of these two variables' effects suggests a stronger role for male colour differences. Together, these results suggest an important role for divergent sexual selection in darter speciation but raise new questions about the mechanisms of sexual selection at play and the role of male nuptial ornaments.     

SEX AND SPECIATION: GENETIC ARCHITECTURE AND EVOLUTIONARY POTENTIAL OF SEXUAL VERSUS NONSEXUAL TRAITS IN THE SIBLING SPECIES OF THE DROSOPHILA MELANOGASTER COMPLEX

Phenotypic divergence in the male reproductive system (genitalia and gonads) between species of the Drosophila melanogaster complex and their hybrids was quantified to decipher the role of these traits in species differentiation and speciation. Internal as well as external, sexual and nonsexual traits were analyzed with respect to genetic variation and trait asymmetry between strains within species, genetic divergence between species, and dominance and asymmetry in species and hybrids. The variation between strains within species was significant among sexual traits, and only external traits were less asymmetric than internal ones, which suggests that sexual traits are not strongly constrained within species. Three main findings show that sexual traits are most divergent between species: (1) testis length and area, and the area of the posterior lobe of the genital arch (sexual traits) showed the highest proportion of variation between species; (2) linear discriminant functions with the highest components associated to sexual traits were better predictors of species membership; and (3) testis length and area revealed a departure from a linear relationship between members of the species group. Examination of interspecific hybrids showed that sexual traits had higher asymmetry in species hybrids than in the parental species and that sexual traits showed additivity or dominance whereas nonsexual traits showed overdominance (with the exception of malpighian tubules length). These results suggest that sexual traits have undergone more genetic changes and, as a result, tend to show higher divergence and stronger hybrid breakdown between species than nonsexual traits. We propose that sexual selection in the broad sense, affecting all aspects of sexuality, may be responsible for the diversified appearance of sexual traits among closely related species and that the genetic architecture underlying sexual traits may be more prone to disruption during the early stages of speciation.     

Regulation of Otx2 expression and its functions in mouse forebrain and midbrain

Otx2 expression in the forebrain and midbrain was found to be regulated by two distinct enhancers (FM and FM2) located at 75 kb 5' upstream and 115 kb 3' downstream. The activities of these two enhancers were absent in anterior neuroectoderm earlier than E8.0; however, at E9.5 their regions of activity spanned the entire mesencephalon and diencephalon with their caudal limits at the boundary with the metencephalon or isthmus. In telencephalon, activities were found only in the dorsomedial aspect. Potential binding sites of OTX and TCF were essential to FM activity, and TCF sites were also essential to FM2 activity. The FM2 enhancer appears to be unique to rodent; however, the FM enhancer region is deeply conserved in gnathostomes. Studies of mutants lacking FM or FM2 enhancer demonstrated that these enhancers indeed regulate Otx2 expression in forebrain and midbrain. Development of mesencephalic and diencephalic regions was differentially regulated in a dose-dependent manner by the cooperation between Otx1 and Otx2 under FM and FM2 enhancers: the more caudal the structure the higher the OTX dose requirement. At E10.5 Otx1-/-Otx2DeltaFM/DeltaFM mutants, in which Otx2 expression under the FM2 enhancer remained, exhibited almost complete loss of the entire diencephalon and mesencephalon; the telencephalon did, however, develop.     

Arginine vasotocin neuronal phenotypes, telencephalic fiber varicosities, and social behavior in butterflyfishes (Chaetodontidae): potential similarities to birds and mammals

The neuropeptide arginine vasopressin (AVP) influences many social behaviors through its action in the forebrain of mammals. However, the function of the homologous arginine vasotocin (AVT) in the forebrain of fishes, specifically the telencephalon remains unresolved. We tested whether the density of AVT-immunoreactive (-ir) fiber varicosities, somata size or number of AVT-ir neuronal phenotypes within the forebrain were predictive of social behavior in reproductive males of seven species of butterflyfishes (family Chaetodontidae) in four phylogenetic clades. Similar to other fishes, the aggressive (often territorial) species in most cases had larger AVT-ir cells within the gigantocellular preoptic cell group. Linear discriminant function analyses demonstrated that the density of AVT-ir varicosities within homologous telencephalic nuclei to those important for social behavior in mammals and birds were predictive of aggressive behavior, social affiliations, and mating system. Of note, the density of AVT-ir varicosities within the ventral nucleus of the ventral telencephalon, thought to be homologous to the septum of other vertebrates, was the strongest predictor of aggressive behavior, social affiliation, and mating system. These results are consistent with the postulate that AVT within the telencephalon of fishes plays an important role in social behavior and may function in a similar manner to that of AVT / AVP in birds and mammals despite having cell populations solely within the preoptic area.     

Differential negative air ion effects on learning disabled and normal-achieving children

Forty normal-achieving and 33 learning disabled (LD) children were assigned randomly to either a negative ion or placebo test condition. On a dichotic listening task using consonant-vowel (CV) combinations, both groups showed an ioninduced increase in the normal right ear advantage (REA). However, the mechanisms for this effect were different for each group. The LDs showed the effect at the right ear/left hemisphere (enhancement). The normal achievers showed the effect at the left ear/right hemisphere (inhibition). The results are consistent with an activation-inhibition model of cerebral function and suggest a functional relationship between arousal, interhemispheric activation-inhibition, and learning disabilities. The LDs may have an interhemispheric dysfunction. Both groups showed superior right ear report and the normal achiever showed overall superiority. Normal achievers showed higher consonant intrusion scores, probably due to a greater cognitive capacity. Age was a significant covariate reflecting developmental capacity changes. Negative air ions are seen to be a tool with potential theoretical and remedial applications.     

The evolution of male infanticide in relation to sexual selection in mammalian carnivores

The evolution of infanticide by males has often been explained by the sexual selection hypothesis, which posits that infanticide improves male reproductive success by shortening the interbirth intervals of the mothers of the killed offspring. In Carnivora, however, the fitness advantages assumed in this hypothesis have been shown in only a few species, and it has been argued that male infanticide may be nonadaptive in pinniped carnivores. According to the sexual selection hypothesis, male infanticide is expected to be more prevalent in species in which males are subjected to stronger sexual selection through intrasexual competition over mates. We examined a phylogenetically corrected relationship between male infanticide and sexual size dimorphism (SSD) as a measure of the intensity of sexual selection in carnivores. Our analyses failed to detect a significant association between the occurrence of male infanticide and SSD across carnivores, although they showed that, among fissipeds (typically terrestrial carnivores), males in species with stronger male-biased SSD are significantly more likely to commit infanticide. This suggests that the evolution of male infanticide is correlated with intense sexual selection in fissipeds. In pinnipeds (Odobenidae, Otariidae, and Phocidae), there was no significant association between male infanticide and SSD. Assuming that SSD represents the intensity of sexual selection on males, this result is consistent with the argument that infanticide by male pinnipeds is not a sexually selected behaviour.     

Change in the developmental fate of the chick optic vesicle from the neural retina to the telencephalon

The forebrain develops into the telencephalon, diencephalon, and optic vesicle (OV). The OV further develops into the optic cup, the inner and outer layers of which develop into the neural retina and retinal pigmented epithelium (RPE), respectively. We studied the change in fate of the OV by using embryonic transplantation and explant culture methods. OVs excised from 10-somite stage chick embryos were freed from surrounding tissues (the surface ectoderm and mesenchyme) and were transplanted back to their original position in host embryos. Expression of neural retina-specific genes, such as Rax and Vsx2 (Chx10), was downregulated in the transplants. Instead, expression of the telencephalon-specific gene Emx1 emerged in the proximal region of the transplants, and in the distal part of the transplants close to the epidermis, expression of an RPE-specific gene Mitf was observed. Explant culture studies showed that when OVs were cultured alone, Rax was continuously expressed regardless of surrounding tissues (mesenchyme and epidermis). When OVs without surrounding tissues were cultured in close contact with the anterior forebrain, Rax expression became downregulated in the explants, and Emx1 expression became upregulated. These findings indicate that chick OVs at stage 10 are bi-potential with respect to their developmental fates, either for the neural retina or for the telencephalon, and that the surrounding tissues have a pivotal role in their actual fates. An in vitro tissue culture model suggests that under the influence of the anterior forebrain and/or its surrounding tissues, the OV changes its fate from the retina to the telencephalon.     

Reproductive skew drives patterns of sexual dimorphism in sponge-dwelling snapping shrimps

Sexual dimorphism is typically a result of strong sexual selection on male traits used in male–male competition and subsequent female choice. However, in social species where reproduction is monopolized by one or a few individuals in a group, selection on secondary sexual characteristics may be strong in both sexes. Indeed, sexual dimorphism is reduced in many cooperatively breeding vertebrates and eusocial insects with totipotent workers, presumably because of increased selection on female traits. Here, we examined the relationship between sexual dimorphism and sociality in eight species of Synalpheus snapping shrimps that vary in social structure and degree of reproductive skew. In species where reproduction was shared more equitably, most members of both sexes were physiologically capable of breeding. However, in species where reproduction was monopolized by a single individual, a large proportion of females—but not males—were reproductively inactive, suggesting stronger reproductive suppression and conflict among females. Moreover, as skew increased across species, proportional size of the major chela—the primary antagonistic weapon in snapping shrimps—increased among females and sexual dimorphism in major chela size declined. Thus, as reproductive skew increases among Synalpheus, female–female competition over reproduction appears to increase, resulting in decreased sexual dimorphism in weapon size.     

Molecular evolution of the sex peptide network in Drosophila

Successful reproduction depends on interactions between numerous proteins beyond those involved directly in gamete fusion. Although such reproductive proteins evolve in response to sexual selection pressures, how networks of interacting proteins arise and evolve as reproductive phenotypes change remains an open question. Here, we investigated the molecular evolution of the ‘sex peptide network’ of Drosophila melanogaster, a functionally well‐characterized reproductive protein network. In this species, the peptide hormone sex peptide (SP) and its interacting proteins cause major changes in female physiology and behaviour after mating. In contrast, females of more distantly related Drosophila species do not respond to SP. In spite of these phenotypic differences, we detected orthologs of all network proteins across 22 diverse Drosophila species and found evidence that most orthologs likely function in reproduction throughout the genus. Within SP‐responsive species, we detected the recurrent, adaptive evolution of several network proteins, consistent with sexual selection acting to continually refine network function. We also found some evidence for adaptive evolution of several proteins along two specific phylogenetic lineages that correspond with increased expression of the SP receptor in female reproductive tracts or increased sperm length, respectively. Finally, we used gene expression profiling to examine the likely degree of functional conservation of the paralogs of an SP network protein that arose via gene duplication. Our results suggest a dynamic history for the SP network in which network members arose before the onset of robust SP‐mediated responses and then were shaped by both purifying and positive selection.