Living fast, dying young: Anthropogenic habitat modification influences the fitness and life history traits of a cooperative breeder.

Anthropogenic habitat modification can indirectly effect reproduction and survival in social species by changing the group structure and social interactions. We assessed the impact of habitat modification on the fitness and life history traits of a cooperative breeder, the Arabian babbler (Argya squamiceps). We collected spatial, reproductive and social data on 572 individuals belonging to 21 social groups over 6 years and combined it with remote sensing to characterize group territories in an arid landscape. In modified resource-rich habitats, groups bred more and had greater productivity, but individuals lived shorter lives than in natural habitats. Habitat modification favoured a faster pace-of-life with lower dispersal and dominance acquisition ages, which might be driven by higher mortality providing opportunities for the dominant breeding positions. Thus, habitat modification might indirectly impact fitness through changes in social structures. This study shows that trade-offs in novel anthropogenic opportunities might offset survival costs by increased productivity.

Fathers and sons, mothers and daughters: Sex-specific genetic architecture for fetal testosterone in a wild mammal.

Testosterone plays a critical role in mediating fitness-related traits in many species. Although it is highly responsive to environmental and social conditions, evidence from several species show a heritable component to its individual variation. Despite the known effects that in utero testosterone exposure have on adult fitness, the heritable component of individual testosterone variation in fetuses is mostly unexplored. Furthermore, testosterone has sex-differential effects on fetal development, i.e., a specific level may be beneficial for male fetuses but detrimental for females, producing sexual conflict. Such sexual conflict may be resolved by the evolution of a sex-specific genetic architecture of the trait. Here, we quantified fetal testosterone levels in a wild species, free-ranging nutrias (Myocastor coypus) using hair-testing and estimated testosterone heritability between parent and offspring from the same and opposite sex. We found that in utero accumulated hair testosterone levels were heritable between parents and offspring of the same sex. Moreover, there was a low additive genetic covariance between the sexes, and a low cross-sex genetic correlation, suggesting a potential for sex-specific trait evolution, expressed early on, in utero.

Paternity share predicts sons' fetal testosterone.

Multiple paternity is common in many species. While its benefits for males are obvious, for females they are less clear. Female indirect benefits may include acquiring 'good genes' for offspring or increasing litter genetic diversity. The nutria (Myocastor coypus) is a successful invasive species. In its native habitat, it is polygynous, with larger and more aggressive males monopolizing paternity. Here, using culled nutria we genetically examined multiple paternity in-utero and found a high incidence of multiple paternity and maintenance of the number of fathers throughout gestation. Moreover, male fetuses sired by the prominent male have higher testosterone levels. Despite being retained, male fetuses of 'rare' fathers, siring commonly only one of the fetuses in the litter, have lower testosterone levels. Considering the reproductive skew of nutria males, if females are selected for sons with higher future reproductive success, low testosterone male fetuses are expected to be selected against. A possible ultimate explanation for maintaining multiple paternity could be that nutria females select for litter genetic diversity e.g., a bet-hedging strategy, even at the possible cost of reducing the reproductive success of some of their sons. Reproductive strategies that maintain genetic diversity may be especially beneficial for invasive species, as they often invade through a genetic bottleneck.

The interaction between cortisol and testosterone predicts leadership within rock hyrax social groups.

Group movement leadership is associated with higher risks for those in the front. Leaders are the first to explore new areas and may be exposed to predation. Individual differences in risk-taking behavior may be related to hormonal differences. In challenging circumstances, such as risk-taking leadership that may pose a cost to the leader, cortisol is secreted both to increase the likelihood of survival by restoring homeostasis, and to mediate cooperative behavior. Testosterone too has a well-established role in risk-taking behavior, and the dual-hormone hypothesis posits that the interaction of testosterone and cortisol can predict social behavior. Based on the dual-hormone hypothesis, we investigated here whether the interaction between testosterone and cortisol can predict risk-taking leadership behavior in wild rock hyraxes (Procavia capensis). We used proximity loggers, observations, and playback trials to characterize hyrax leaders in three different leadership contexts that varied in their risk levels. In support of the dual-hormone hypothesis, we found that cortisol and testosterone interactions predict leadership that involves risk. Across different circumstances that involved low or high levels of risk, testosterone was positively related to leadership, but only in individuals (both males and females) with low levels of cortisol. We also found an interaction between these hormone levels and age at the low-risk scenarios. We suggest that the close social interactions and affiliative behavior among hyrax females within small egalitarian groups may make female leadership less risky, and therefore less stressful, and allow female leaders to influence group activities.

Free-living gerbils with higher testosterone take fewer risks.

Among the physiological differences between the sexes are circulating androgen levels. Testosterone (T) is an androgen that has been linked to aggression and risk-taking in male vertebrates, so that males with higher T are generally more aggressive and take more risks. In females, T is not often measured, and its relationship with behaviour has been less studied. The costs of elevated T are assumed to be higher for reproductive females, while the benefits higher for males. Here, we tested the association between endogenous T and risk-taking behaviours in both males and females under well-studied experimental settings in free-living Baluchistan gerbils (Gerbillus nanus; Gn). In addition, we experimentally elevated Gn T levels using implants and measured risk-taking behaviour. Surprisingly, we found that there were no differences in the association between T and risk-taking behaviours between males and females, and that in both sexes, Gn with higher T levels took fewer risks. We also found that Gn spent equal time foraging between risky (open habitat) and safe (under a bush) experimental food patches. We expected Gn, which are nocturnal, to take fewer risks during full moon nights, but found that Gn were more active during moon lit nights than during dark (new moon) nights. This study demonstrates that T has many functions, and that its effects are complex and often unpredictable. It also shows that hypotheses regarding the propensity to take risks under specific coverage and light regimes are not universal, and likely include variables such as species, environment, context, and predator-specific behavioural strategies.

Continuity of psychopathology v. resilience across the transition to adolescence: role of hair cortisol and sensitive caregiving.

BACKGROUND: The transition to adolescence implicates heightened vulnerability alongside increased opportunities for resilience. Contexts of early life stress (ELS) exacerbate risk; still, little research addressed biobehavioral mediators of risk and resilience across the adolescent transition following ELS. Utilizing a unique cohort, we tested biosocial moderators of chronicity in adolescents' internalizing disorders v. resilience. METHOD: Families exposed to chronic war-related trauma, v. controls, were followed. We utilized data from three time-points framing the adolescent transition: late childhood (N = 177, Mage = 9.3 years ± 1.41), early adolescence (N = 111, Mage = 11 0.66 years ± 1.23), and late adolescence (N = 138, Mage = 15.65 years ± 1.31). In late childhood and late adolescence children's internalizing disorders were diagnosed. At early adolescence maternal and child's hair cortisol concentrations (HCC), maternal sensitivity, and mothers' post-traumatic symptoms evaluated. RESULTS: War-exposed children exhibited more internalizing disorders of chronic trajectory and mothers were less sensitive and more symptomatic. Three pathways elucidated the continuity of psychopathology: (a) maternal sensitivity moderated the risk of chronic psychopathology, (b) maternal post-traumatic symptoms mediated continuity of risk, (c) trauma exposure moderated the association between child internalizing disorders at late childhood and maternal HCC, which linked with child HCC. Child HCC linked with maternal post-traumatic symptoms, which were associated with child disorders in late adolescence. CONCLUSION: Results demonstrate the complex interplay of maternal and child's biosocial factors as mediators and moderators of risk chronicity across the adolescent transition following trauma. Findings are first to utilize maternal and child's HCC as biomarkers of chronic stress v. resilience during adolescence, a period of neural reorganization and personal growth that shapes the individual's lifetime adaptation.

Male rock hyraxes that maintain an isochronous song rhythm achieve higher reproductive success.

Rhythmic stability (nonrandom temporal structure) is required for many neural and physiological functions, whereas rhythmic irregularities can indicate genetic or developmental deficiencies. Therefore, rhythmic courtship or contest signals are widespread in nature as honest advertisement displays. Examination of bird songs revealed the pervasiveness of categorical rhythmic patterns that can be described as small integer ratios between sequential inter-call intervals. As similar rhythmic profiles are prevalent in human music, it was suggested that a shared functionality could drive both animal songs and human musical rhythms, facilitating synchrony between signallers and enabling easy identification of performance errors. Here we examined whether the rhythmic structure and the rhythmic stability of vocal displays are related to reproductive success in male rock hyraxes (Procavia capensis), which presents an unusual case of a terrestrial singing mammal. We combined long-term parentage analysis of 13 male hyraxes (22 male/years) with an analysis of an audio library of 105 hyrax songs. Male annual reproductive success was determined by the number of offspring that survived to the age of 1 year. The frequency of singing events was used to determine the seasonal singing effort for each male. Songs were analysed for rhythmic structure, focusing on the presence of categorical rhythms and the contribution of rhythmic stability to annual reproductive success. We found that male hyraxes that sing more frequently tend to have more surviving offspring and that the rhythmic profile of hyrax songs is predominantly isochronous with sequential vocal element pairs nearly equally spaced. The ratio of isochronous vocal element transitions (on-integer) to element transitions that deviate from an isochronous pattern (off-integer) in hyrax songs is positively correlated with male reproductive success. Our findings support the notion that isochronous rhythmic stability can serve as an indication of quality in sexually selected signals and is not necessarily driven by the need for multiple caller synchronization. The relative scarcity of nonisochronous rhythmic categories in individually performed hyrax songs raises the question of whether such rhythmic categories could be a product of collective, coordinated signalling, while being selected against in individual performance.

High-resolution tracking of hyrax social interactions highlights nighttime drivers of animal sociality.

Network structure is a key driver of animal fitness, pathogen transmission, information spread, and population demographics in the wild. Although a considerable body of research applied network analysis to animal societies, only little effort has been devoted to separate daytime and nighttime sociality and explicitly test working hypotheses on social structures emerging at night. Here, we investigated the nighttime sociality of a wild population of rock hyraxes (Procavia capensis) and its relation to daytime social structure. We recorded nearly 15,000 encounters over 27 consecutive days and nights using proximity loggers. Overall, we show that hyraxes are more selective of their social affiliates at night compared to daytime. We also show that hyraxes maintain their overall network topology while reallocating the weights of social relationships at the daily and monthly scales, which could help hyraxes maintain their social structure over long periods while adapting to local constraints and generate complex social dynamics. These results suggest that complex network dynamics can be a by-product of simple daily social tactics and do not require high cognitive abilities. Our work sheds light on the function of nighttime social interactions in diurnal social species.

Sex-associated and context-dependent leadership in the rock hyrax.

In many mammalian species, both sexes may take leadership role, but different traits may play a role in determining variation within species. Here we examine the effect of sex on leadership. We present three complementary datasets derived from a well-studied population of wild rock hyrax (Procavia capensis). The findings demonstrated that male and female rock hyraxes take on different leadership positions, depending on the context. When risk is moderate, more likely to lead are younger resident males, which experience high cortisol and lower testosterone levels. However, during acute predation scenarios, more likely to lead are males with lower centrality status. We suggest that hyrax males exhibit risky behaviors that may reflect their need for self-advertisement. In contrast, leadership among group females is more equally distributed. Females have little to gain from risky actions due to the lack of competition among them, but nonetheless take leadership positions.

Attentional networks during the menstrual cycle.

The menstrual cycle is characterized partially by fluctuations of the ovarian hormones estradiol (E2) and progesterone (P4), which are implicated in the regulation of cognition. Research on attention in the different stages of the menstrual cycle is eclectic with discrepancies in attention definitions, and the three attentional networks (alerting, orienting and executive) and their interaction were not explored during the menstrual cycle. In the current study, we used the ANT-I (attentional network test - interactions) to examine naturally cycling women (NC) and women using oral contraceptives (OC). We tested their performance at two time points that fit, in natural cycles, the follicular phase and the luteal phase. We found no differences in performance between the two time points (day 4 / day 18) for the OC group: the response pattern replicated known ANT-I findings. However, the NC group showed differences between the two time points. In the follicular phase, responses replicated known ANT-I results, but in the luteal phase, alertness did not interact with executive and orienting networks, resulting in a larger congruency effect (executive network) when attention was not oriented to the target in alerting and no alerting conditions. Results-driven exploratory regression analysis of E2 and P4 suggested that change in P4 from the follicular phase/day 4 to the luteal phase/day 18 was a mediator for the alerting effect found between groups. In conclusion, the alerting state, found with or without alertness manipulation, suggests that there is a progesterone-mediated activation of the alerting system during the luteal phase.

Residential greenness and hair cortisol levels during the first trimester of pregnancy.

BACKGROUND AND AIM: Studies have shown that increased maternal cortisol level is associated with child adverse health outcomes. Hair cortisol (HC) is suitable for assessing long-term circulating cortisol concentration. Only two previous studies reported beneficial associations between cortisol and residential greenness during pregnancy and no study focused on the first trimester. Our aim was to evaluate the association between residential greenness and first trimester HC levels among pregnant women in Israel. METHODS: Women were recruited during second and third trimesters. Hair samples were collected from the scalp and retrospective HC levels during the first trimester were quantified for 217 women. HC levels were natural log transformed and outliers were excluded. Based on geocoded birth address, small area sociodemographic status (SES) and mean residential surrounding greenness were calculated using high-resolution satellite-based Normalised Difference Vegetation Index (NDVI) data at 100, 300 and 500-m buffers in a cross-sectional approach. In addition, longitudinal exposure to mean greenness during a week preconception and during the first trimester were calculated. Missing covariates were imputed and linearity of the associations were evaluated. Generalized linear models were used to estimate the crude and adjusted associations controlled for the relevant covariates. RESULTS: After exclusion of outliers, for 211 women, crude and adjusted beneficial associations between exposure to higher mean NDVI and HC levels were observed for all the exposure measures. An increase in 1 interquartile range of greenness (100 m buffer) was associated with a statistically significant lower estimated natural log mean HC level (-0.27 95% CI: -0.44; -0.11). The associations were robust to adjustment for covariates. The findings were consistent for different buffers, for the longitudinal approach, when all observations were included in the analysis and slightly stronger associations were observed for women with addresses geocoded at the home or street level. For most of the exposure measures, stronger associations were observed among those of lower sociodemographic status. CONCLUSION: Our findings that more greenness associated with reduced maternal cortisol levels measured in the hair during the first trimester, could have substantial implications for urban planners and public health professional. If our observations will be replicated, it may present a useful avenue for public-health intervention to promote health through the provision of greenness exposure during early pregnancy, specifically to disadvantage populations.

Do boars compensate for hunting with higher reproductive hormones?

The predation-stress hypothesis has been proposed as a general mechanism to explain the negative effect of predation risk on reproduction, through a chronic activation of the stress response. However, in some cases, stress appears to augment the reproductive potential of mammals. Wild boar (Sus scrofa) populations are on a rise worldwide, despite the high hunting pressure that they are exposed to. This hunting pressure instigates, among other effects, earlier sexual maturity in juvenile females, leading to the shortening of wild boars' generation time. The mechanism that underlies this earlier sexual maturity under high hunting pressure has not been examined to date. To explore the physiological effects that hunting has on the reproductive system and whether the stress response is involved, we examined steroid hormone levels in the hair of female wild boars in northern Israel, comparing populations exposed to high and low hunting pressure. Furthermore, we compared steroid levels in the hair of female wild boars that were roaming alone or as a part of a group. We found no hormonal signs of stress in the hunted boars. Cortisol levels were low in both the high and low hunting-pressure groups. Yet, progesterone levels were higher in females that were exposed to high hunting pressure. Females roaming in a group also had higher progesterone levels compared to females that were alone, with no distinguishable differences in cortisol levels. These elevations in reproductive hormones that were associated with hunting may lead to a higher reproductive potential in female wild boars. They further show that high hunting pressure does not necessarily lead to chronic stress that impairs the reproductive potential of female wild boars. This data suggests that a reproductive hormonal response may be one of the factors leading to the rapid wild boars population growth worldwide, despite the high hunting pressure.

Evolution of Embryo Implantation Was Enabled by the Origin of Decidual Stromal Cells in Eutherian Mammals.

Mammalian pregnancy evolved in the therian stem lineage, that is, before the common ancestor of marsupials and eutherian (placental) mammals. Ancestral therian pregnancy likely involved a brief phase of attachment between the fetal and maternal tissues followed by parturition-similar to the situation in most marsupials including the opossum. In all eutherians, however, embryo attachment is followed by implantation, allowing for a stable fetal-maternal interface and an extended gestation. Embryo attachment induces an attachment reaction in the uterus that is homologous to an inflammatory response. Here, we elucidate the evolutionary mechanism by which the ancestral inflammatory response was transformed into embryo implantation in the eutherian lineage. We performed a comparative uterine transcriptomic and immunohistochemical study of three eutherians, armadillo (Dasypus novemcinctus), hyrax (Procavia capensis), and rabbit (Oryctolagus cuniculus); and one marsupial, opossum (Monodelphis domestica). Our results suggest that in the eutherian lineage, the ancestral inflammatory response was domesticated by suppressing one of its modules detrimental to pregnancy, namely, neutrophil recruitment by cytokine IL17A. Further, we propose that this suppression was mediated by decidual stromal cells, a novel cell type in eutherian mammals. We tested a prediction of this model in vitro and showed that decidual stromal cells can suppress the production of IL17A from helper T cells. Together, these results provide a mechanistic understanding of early stages in the evolution of eutherian pregnancy.

Sex differences in testosterone reactivity and sensitivity in a non-model gerbil.

Although testosterone (T) is a key regulator in vertebrate development, physiology, and behaviour in both sexes, studies suggest that its regulation may be sex-specific. We measured circulating T levels in Baluchistan gerbils (Gerbillus nanus) in the field and in the lab all year round and found no significant sex differences. However, we observed sex differences in circulating T levels following gonadotropin-releasing hormone (GnRH) challenge and T implants in this non-model species. Whereas only males elevated T following a GnRH challenge, females had higher serum T concentrations following T implant insertion. These differences may be a result of different points of regulation along the hypothalamic-pituitary-gonadal (HPG) axis. Consequently, we examined sex differences in the mRNA expression of the androgen receptor (AR) in multiple brain regions. We identified AR and ß-actin sequences in assembled genomic sequences of members of the Gerbillinae, which were analogous to rat sequences, and designed primers for them. The distribution of the AR in G. nanus brain regions was similar to documented expression profiles in rodents. We found lower AR mRNA levels in females in the striatum. Additionally, G. nanus that experienced housing in mixed-sex pairs had higher adrenal AR expression than G. nanus that were housed alone. Regulation of the gerbil HPG axis may reflect evolutionary sex differences in life-history strategies, with males ready to reproduce when receptive females are available, while the possible reproductive costs associated with female T direct its regulation upstream.

Physiological and economic benefits of abandoning invasive surgical procedures and enhancing animal welfare in swine production.

Food-animal welfare is a major ethical and social concern. Pork is the most consumed meat worldwide, with over a billion pigs slaughtered annually. Most of these pigs routinely undergo painful surgical procedures (surgical castration, tail docking, teeth clipping), which farmers often reluctant to avoid, claiming it would increase cost and reduce production efficiency. Herein, this study indicates that these procedures compromise pigs' health and condition. Replacing surgical castration with immunocastration, avoiding tail docking and teeth clipping, and providing environmental enrichment, resulted in significant increase in weight gain, lowered risks for injuries and death, and reduced saliva and hair cortisol, both biomarkers for stress. Testosterone and DHEA analyses confirmed that immunocastration was an effective alternative to surgical castration. Economic models for the entire US swine market revealed that following across-the-board acceptance of this management, pork meat price is expected to drop, while the total annual social welfare (combined consumer and producer surplus) is expected to increase by $US 1.48 to 1.92 billion. In conclusion, sustainable swine farming management can be beneficial for both animals and farmers. Applying such welfare-friendly management is expected to reduce stress, enhance piglet/pig welfare and production, and improve the economics of swine operations in the global agro-food system.

Social context mediates testosterone's effect on snort acoustics in male hyrax songs.

Testosterone affects physical and motivational states, both of which may strongly influence vocalization structure and acoustics. The loud complex calls (i.e., songs) of male rock hyraxes (Procavia capensis) are used as honest signals for advertising physical and social states. The snort, a low frequency, noisy element of the song, encodes information on the singer's age and social rank via harshness, as measured by jitter (i.e., acoustic frequency stability) and duration; suggesting that the snort concomitantly advertises both vocal stability and aggression. Our past findings revealed that testosterone levels are related to both vocal elements and social status of male hyraxes, suggesting that hormonal mechanisms mediate the motivation for aggressive and courtship behaviors. Here we examined whether long-term androgen levels are related to snort acoustics and song structure by comparing levels of testosterone in hair with acoustic and structural parameters. We found that songs performed by individuals with higher testosterone levels include more singing bouts and longer, smoother snorts, but only in those songs induced by external triggers. It is possible that hyraxes with higher levels of testosterone possess the ability to perform higher-quality singing, but only invest in situations of high social arousal and potential benefit. Surprisingly, in spontaneous songs, hyraxes with high testosterone were found to snort more harshly than low-testosterone males. The context dependent effects of high testosterone on snort acoustics suggest that the aggressive emotional arousal associated with testosterone is naturally reflected in the jittery hyrax snort, but that it can be masked by high-quality performance.

Non-model species deliver a non-model result: Nutria female fetuses neighboring males in utero have lower testosterone.

Neighboring fetuses may impact their siblings in various respects, depending on their in utero location and sex. The effects of the intrauterine position (IUP) are widely studied in model organisms, especially laboratory bred murine strains that are characterized by short gestations and altricial offspring. In some species, the proximity to a male fetus and its higher circulating testosterone masculinizes neighboring female fetuses. In utero testosterone exposure might be manifested as higher testosterone concentrations, which contribute to a variation in morphology, reproductive potential and behavior. In this study, we examined the influence of neighboring an opposite sex fetus on testosterone levels in a feral animal model characterized by a long gestation and precocious offspring. Using necropsies of culled nutria (Myocastor coypus), we accurately determined the IUP and quantified testosterone immunoreactivity in fetal hair. We found that as expected, both male and female fetuses neighboring a male in utero had longer anogenital distance. However, females adjacent to males in utero showed lower testosterone levels than male fetuses, while testosterone levels of females without a male neighbor did not differ from those of males. This surprising result suggests an alternative mode by which local exogenous steroids may modify the local fetal environment. Our study emphasizes the importance of examining known phenomena in species with different life histories, other than the traditional murine models, to enhance our understanding of the evolutionary mechanisms that are driving sexual differentiation.

Can hair steroids predict pregnancy longevity?

Maintaining pregnancy to term is important as preterm delivery is a risk factor for impaired infant development, which may have negative long-term consequences. Therefore, developing biomarkers that can predict pregnancy longevity during early gestation is essential for the prevention of preterm birth. Here we explored whether maternal hair testosterone and cortisol, representing the pre-conception and first trimester periods respectively, may be used to predict pregnancy longevity. We recruited 125 pregnant women that contributed hair samples and answered a personal information questionnaire that included pre-conception smoking. We quantified steroids using commercial enzyme-linked immunosorbent assay kits. Gestational age at delivery was obtained from medical records. We used General Linear Models to predict gestation length. The model that included first trimester cortisol, pre-conception smoking, pre-conception testosterone and the interaction between first trimester cortisol and pre-conception smoking predicted 13% of the variance in gestation length (R2 = 0.130; n = 105; p = 0.007). First trimester cortisol was the best predictor of gestational length. Women with high levels of cortisol in their first trimester had an increased probability of a full-term delivery. The effect of cortisol was especially pronounced in smokers (ß = 1.69), compared to non-smokers (ß = 0.45). Pre-conception testosterone also contributed to the model. Our study suggests that hair steroids may be used to predict pregnancy longevity, together with other contributing factors.

Is there an association between maternal anxiety propensity and pregnancy outcomes?

BACKGROUND: Several studies have shown inconsistent associations between anxiety during pregnancy and adverse pregnancy outcome. This inconsistency may be due to lack of controlling for the timing and type of maternal anxiety. We aimed to isolate a specific type of anxiety - maternal anxiety propensity, which is not directly related to pregnancy, and evaluate its association with adverse pregnancy outcome. METHODS: We conducted a prospective observational study of 512 pregnant women, followed to delivery. The trait anxiety scale of the State-Trait Anxiety Inventories was used in order to detect a propensity towards anxiety. The association between anxiety propensity (defined as trait-anxiety subscale score above 38) and adverse pregnancy outcome was evaluated. Primary outcome was a composite outcome including preterm birth prior to 37 gestational weeks, hypertensive disorders in pregnancy, small for gestational age newborn and gestational diabetes mellitus. Secondary outcomes were each one of the above mentioned gestational complications. RESULTS: There were no significant between-group differences in adverse pregnancy outcomes, including the rate of preterm birth, hypertensive disorders, small for gestational age, gestational diabetes or a composite outcome of them all. CONCLUSION: Anxiety propensity is not associated with adverse pregnancy outcome.