Journal: Current biology : CB
The history of humankind is marked by the constant adoption of new dietary habits affecting human physiology, metabolism, and even the development of nutrition-related disorders. Despite clear archaeological evidence for the shift from hunter-gatherer lifestyle to agriculture in Neolithic Europe , very little information exists on the daily dietary habits of our ancestors. By undertaking a complementary -omics approach combined with microscopy, we analyzed the stomach content of the Iceman, a 5,300-year-old European glacier mummy [2, 3]. He seems to have had a remarkably high proportion of fat in his diet, supplemented with fresh or dried wild meat, cereals, and traces of toxic bracken. Our multipronged approach provides unprecedented analytical depth, deciphering the nutritional habit, meal composition, and food-processing methods of this Copper Age individual.
Balance arises from the interplay of external forces acting on the body and internally generated movements. Many animal bodies are inherently unstable, necessitating corrective locomotion to maintain stability. Understanding how developing animals come to balance remains a challenge. Here we study the interplay among environment, sensation, and action as balance develops in larval zebrafish. We first model the physical forces that challenge underwater balance and experimentally confirm that larvae are subject to constant destabilization. Larvae propel in swim bouts that, we find, tend to stabilize the body. We confirm the relationship between locomotion and balance by changing larval body composition, exacerbating instability and eliciting more frequent swimming. Intriguingly, developing zebrafish come to control the initiation of locomotion, swimming preferentially when unstable, thus restoring preferred postures. To test the sufficiency of locomotor-driven stabilization and the developing control of movement timing, we incorporate both into a generative model of swimming. Simulated larvae recapitulate observed postures and movement timing across early development, but only when locomotor-driven stabilization and control of movement initiation are both utilized. We conclude the ability to move when unstable is the key developmental improvement to balance in larval zebrafish. Our work informs how emerging sensorimotor ability comes to impact how and why animals move when they do.
Ants can navigate over long distances between their nest and food sites using visual cues [1, 2]. Recent studies show that this capacity is undiminished when walking backward while dragging a heavy food item [3-5]. This challenges the idea that ants use egocentric visual memories of the scene for guidance [1, 2, 6]. Can ants use their visual memories of the terrestrial cues when going backward? Our results suggest that ants do not adjust their direction of travel based on the perceived scene while going backward. Instead, they maintain a straight direction using their celestial compass. This direction can be dictated by their path integrator  but can also be set using terrestrial visual cues after a forward peek. If the food item is too heavy to enable body rotations, ants moving backward drop their food on occasion, rotate and walk a few steps forward, return to the food, and drag it backward in a now-corrected direction defined by terrestrial cues. Furthermore, we show that ants can maintain their direction of travel independently of their body orientation. It thus appears that egocentric retinal alignment is required for visual scene recognition, but ants can translate this acquired directional information into a holonomic frame of reference, which enables them to decouple their travel direction from their body orientation and hence navigate backward. This reveals substantial flexibility and communication between different types of navigational information: from terrestrial to celestial cues and from egocentric to holonomic directional memories.
Climate change and fisheries are transforming the oceans, but we lack a complete understanding of their ecological impact [1-3]. Environmental degradation can cause maladaptive habitat selection, inducing ecological traps with profound consequences for biodiversity [4-6]. However, whether ecological traps operate in marine systems is unclear . Large marine vertebrates may be vulnerable to ecological traps , but their broad-scale movements and complex life histories obscure the population-level consequences of habitat selection [8, 9]. We satellite tracked postnatal dispersal in African penguins (Spheniscus demersus) from eight sites across their breeding range to test whether they have become ecologically trapped in the degraded Benguela ecosystem. Bayesian state-space and habitat models show that penguins traversed thousands of square kilometers to areas of low sea surface temperatures (14.5°C-17.5°C) and high chlorophyll-a (∼11 mg m(-3)). These were once reliable cues for prey-rich waters, but climate change and industrial fishing have depleted forage fish stocks in this system [10, 11]. Juvenile penguin survival is low in populations selecting degraded areas, and Bayesian projection models suggest that breeding numbers are ∼50% lower than if non-impacted habitats were used, revealing the extent and effect of a marine ecological trap for the first time. These cascading impacts of localized forage fish depletion-unobserved in studies on adults-were only elucidated via broad-scale movement and demographic data on juveniles. Our results support suspending fishing when prey biomass drops below critical thresholds [12, 13] and suggest that mitigation of marine ecological traps will require matching conservation action to the scale of ecological processes .
Why females of some species cease ovulation prior to the end of their natural lifespan is a long-standing evolutionary puzzle [1-4]. The fitness benefits of post-reproductive helping could in principle select for menopause [1, 2, 5], but the magnitude of these benefits appears insufficient to explain the timing of menopause [6-8]. Recent theory suggests that the cost of inter-generational reproductive conflict between younger and older females of the same social unit is a critical missing term in classical inclusive fitness calculations (the “reproductive conflict hypothesis” [6, 9]). Using a unique long-term dataset on wild resident killer whales, where females can live decades after their final parturition, we provide the first test of this hypothesis in a non-human animal. First, we confirm previous theoretical predictions that local relatedness increases with female age up to the end of reproduction. Second, we construct a new evolutionary model and show that given these kinship dynamics, selection will favor younger females that invest more in competition, and thus have greater reproductive success, than older females (their mothers) when breeding at the same time. Third, we test this prediction using 43 years of individual-based demographic data in resident killer whales and show that when mothers and daughters co-breed, the mortality hazard of calves from older-generation females is 1.7 times that of calves from younger-generation females. Intergenerational conflict combined with the known benefits conveyed to kin by post-reproductive females can explain why killer whales have evolved the longest post-reproductive lifespan of all non-human animals.
Countershading was one of the first proposed mechanisms of camouflage [1, 2]. A dark dorsum and light ventrum counteract the gradient created by illumination from above, obliterating cues to 3D shape [3-6]. Because the optimal countershading varies strongly with light environment [7-9], pigmentation patterns give clues to an animal’s habitat. Indeed, comparative evidence from ungulates  shows that interspecific variation in countershading matches predictions: in open habitats, where direct overhead sunshine dominates, a sharp dark-light color transition high up the body is evident; in closed habitats (e.g., under forest canopy), diffuse illumination dominates and a smoother dorsoventral gradation is found. We can apply this approach to extinct animals in which the preservation of fossil melanin allows reconstruction of coloration [10-15]. Here we present a study of an exceptionally well-preserved specimen of Psittacosaurus sp. from the Chinese Jehol biota [16, 17]. This Psittacosaurus was countershaded  with a light underbelly and tail, whereas the chest was more pigmented. Other patterns resemble disruptive camouflage, whereas the chin and jugal bosses on the face appear dark. We projected the color patterns onto an anatomically accurate life-size model in order to assess their function experimentally. The patterns are compared to the predicted optimal countershading from the measured radiance patterns generated on an identical uniform gray model in direct versus diffuse illumination. These studies suggest that Psittacosaurus sp. inhabited a closed habitat such as a forest with a relatively dense canopy. VIDEO ABSTRACT.
Bright-red colors in vertebrates are commonly involved in sexual, social, and interspecific signaling [1-8] and are largely produced by ketocarotenoid pigments. In land birds, ketocarotenoids such as astaxanthin are usually metabolically derived via ketolation of dietary yellow carotenoids [9, 10]. However, the molecular basis of this gene-environment mechanism has remained obscure. Here we use the yellowbeak mutation in the zebra finch (Taeniopygia guttata) to investigate the genetic basis of red coloration. Wild-type ketocarotenoids were absent in the beak and tarsus of yellowbeak birds. The yellowbeak mutation mapped to chromosome 8, close to a cluster of cytochrome P450 loci (CYP2J2-like) that are candidates for carotenoid ketolases. The wild-type zebra finch genome was found to have three intact genes in this cluster: CYP2J19A, CYP2J19B, and CYP2J40. In yellowbeak, there are multiple mutations: loss of a complete CYP2J19 gene, a modified remaining CYP2J19 gene (CYP2J19(yb)), and a non-synonymous SNP in CYP2J40. In wild-type birds, CYP2J19 loci are expressed in ketocarotenoid-containing tissues: CYP2J19A only in the retina and CYP2J19B in the beak and tarsus and to a variable extent in the retina. In contrast, expression of CYP2J19(yb) is barely detectable in the beak of yellowbeak birds. CYP2J40 has broad tissue expression and shows no differences between wild-type and yellowbeak. Our results indicate that CYP2J19 genes are strong candidates for the carotenoid ketolase and imply that ketolation occurs in the integument in zebra finches. Since cytochrome P450 enzymes include key detoxification enzymes, our results raise the intriguing possibility that red coloration may be an honest signal of detoxification ability.
An aversion to harming others is a core component of human morality and is disturbed in antisocial behavior [1-4]. Deficient harm aversion may underlie instrumental and reactive aggression, which both feature in psychopathy . Past work has highlighted monoaminergic influences on aggression [6-11], but a mechanistic account of how monoamines regulate antisocial motives remains elusive. We previously observed that most people show a greater aversion to inflicting pain on others than themselves . Here, we investigated whether this hyperaltruistic disposition is susceptible to monoaminergic control. We observed dissociable effects of the serotonin reuptake inhibitor citalopram and the dopamine precursor levodopa on decisions to inflict pain on oneself and others for financial gain. Computational models of choice behavior showed that citalopram increased harm aversion for both self and others, while levodopa reduced hyperaltruism. The effects of citalopram were stronger than those of levodopa. Crucially, neither drug influenced the physical perception of pain or other components of choice such as motor impulsivity or loss aversion [13, 14], suggesting a direct and specific influence of serotonin and dopamine on the valuation of harm. We also found evidence for dose dependency of these effects. Finally, the drugs had dissociable effects on response times, with citalopram enhancing behavioral inhibition and levodopa reducing slowing related to being responsible for another’s fate. These distinct roles of serotonin and dopamine in modulating moral behavior have implications for potential treatments of social dysfunction that is a common feature as well as a risk factor for many psychiatric disorders.
Internal action models (IAMs) are brain templates for sensory-motor coordination underlying diverse behaviors . An emerging theory suggests that impaired IAMs are a common theme in autism spectrum disorder (ASD) [2-4]. However, whether impaired IAMs occur across sensory systems and how they relate to the major phenotype of ASD, namely impaired social communication , remains unclear. Olfaction relies on an IAM known as the sniff response, where sniff magnitude is automatically modulated to account for odor valence [6-12]. To test the failed IAM theory in olfaction, we precisely measured the non-verbal non-task-dependent sniff response concurrent with pleasant and unpleasant odors in 36 children-18 with ASD and 18 matched typically developing (TD) controls. We found that whereas TD children generated a typical adult-like sniff response within 305 ms of odor onset, ASD children had a profoundly altered sniff response, sniffing equally regardless of odor valance. This difference persisted despite equal reported odor perception and allowed for 81% correct ASD classification based on the sniff response alone (binomial, p < 0.001). Moreover, increasingly aberrant sniffing was associated with increasingly severe ASD (r = -0.75, p < 0.001), specifically with social (r = -0.72, p < 0.001), but not motor (r < -0.38, p > 0.18), impairment. These results uncover a novel ASD marker implying a mechanistic link between the underpinnings of olfaction and ASD and directly linking an impaired IAM with impaired social abilities.
Social touch plays a powerful role in human life, with important physical and mental health benefits in development and adulthood. Touch is central in building the foundations of social interaction, attachment, and cognition [1-5], and early, social touch has unique, beneficial neurophysiological and epigenetic effects [6-9]. The recent discovery of a separate neurophysiological system for affectively laden touch in humans has further kindled scientific interest in the area [10, 11]. Remarkably, however, little is known about what motivates and sustains the human tendency to touch others in a pro-social manner. Given the importance of social touch, we hypothesized that active stroking elicits more sensory pleasure when touching others' skin than when touching one’s own skin. In a set of six experiments (total N = 133) we found that healthy participants, mostly tested in pairs to account for any objective differences in skin softness, consistently judged another’s skin as feeling softer and smoother than their own skin. We further found that this softness illusion appeared selectively when the touch activated a neurophysiological system for affective touch in the receiver. We conclude that this sensory illusion underlies a novel, bodily mechanism of socio-affective bonding and enhances our motivation to touch others.