Amphicarpic development in Cardamine chenopodiifolia.

Amphicarpy is an unusual trait where two fruit types develop on the same plant: one above and the other belowground. This trait is not found in conventional model species. Therefore, its development and molecular genetics remain under-studied. Here, we establish the allooctoploid Cardamine chenopodiifolia as an emerging experimental system to study amphicarpy. We characterized C. chenopodiifolia development, focusing on differences in morphology and cell wall histochemistry between above- and belowground fruit. We generated a reference transcriptome with PacBio full-length transcript sequencing and analysed differential gene expression between above- and belowground fruit valves. Cardamine chenopodiifolia has two contrasting modes of seed dispersal. The main shoot fails to bolt and initiates floral primordia that grow underground where they self-pollinate and set seed. By contrast, axillary shoots bolt and develop exploding seed pods aboveground. Morphological differences between aerial explosive fruit and subterranean nonexplosive fruit were reflected in a large number of differentially regulated genes involved in photosynthesis, secondary cell wall formation and defence responses. Tools established in C. chenopodiifolia, such as a reference transcriptome, draft genome assembly and stable plant transformation, pave the way to study amphicarpy and trait evolution via allopolyploidy.

Individual differences in sociocognitive traits in semi-free-ranging rhesus monkeys (Macaca mulatta).

Characterizing individual differences in cognition is crucial for understanding the evolution of cognition as well as to test the biological consequences of different cognitive traits. Here, we harnessed the strengths of a uniquely large, naturally-living primate population at the Cayo Santiago Biological Field Station to characterized individual differences in rhesus monkey performance across two social cognitive tasks. A total of n = 204 semi-free-ranging adult rhesus monkeys participated in a data collection procedure, where we aimed to test individuals on both tasks at two time-points that were one year apart. In the socioemotional responses task, we assessed monkeys' attention to conspecific photographs with neutral versus negative emotional expressions. We found that monkeys showed overall declines in interest in conspecific photographs with age, but relative increases in attention to threat stimuli specifically, and further that these responses exhibited long-term stability across repeated testing. In the gaze following task we assessed monkeys' propensity to co-orient with an experimenter. Here, we found no evidence for age-related change in responses, and responses showed only limited repeatability over time. Finally, we found some evidence for common individual variation for performance across the tasks: monkeys that showed greater interest in conspecific photographs were more likely to follow a human's gaze. These results show how studies of comparative cognitive development and aging can provide insights into the evolution of cognition, and identify core primate social cognitive traits that may be related across and within individuals.

The origins of cognitive flexibility in chimpanzees.

Cognitive flexibility is a core component of executive function, a suite of cognitive capacities that enables individuals to update their behavior in dynamic environments. Human executive functions are proposed to be enhanced compared to other species, but this inference is based primarily on neuroanatomical studies. To address this, we examined the nature and origins of cognitive flexibility in chimpanzees, our closest living relatives. Across three studies, we examined different components of cognitive flexibility using reversal learning tasks where individuals first learned one contingency and then had to shift responses when contingencies flipped. In Study 1, we tested n = 82 chimpanzees ranging from juvenility to adulthood on a spatial reversal task, to characterize the development of basic shifting skills. In Study 2, we tested how n = 24 chimpanzees use spatial versus arbitrary perceptual information to shift, a proposed difference between human and nonhuman cognition. In Study 3, we tested n = 40 chimpanzees on a probabilistic reversal task. We found an extended developmental trajectory for basic shifting and shifting in response to probabilistic feedback-chimpanzees did not reach mature performance until late in ontogeny. Additionally, females were faster to shift than males were. We also found that chimpanzees were much more successful when using spatial versus perceptual cues, and highly perseverative when faced with probabilistic versus consistent outcomes. These results identify both core features of chimpanzee cognitive flexibility that are shared with humans, as well as constraints on chimpanzee cognitive flexibility that may represent evolutionary changes in human cognitive development.

Whispers from vestigial nubbins: Arrested development provokes trait loss in toads.

Despite the use of acoustic communication, many species of toads (family Bufonidae) have lost parts of the tympanic middle ear, representing at least 12 independent evolutionary occurrences of trait loss. The comparative development of the tympanic middle ear in toads is poorly understood. Here, we compared middle ear development among two pairs of closely related toad species in the genera Atelopus and Rhinella that have (eared) or lack (earless) middle ear structures. We bred toads in Peru and Ecuador, preserved developmental series from tadpoles to juveniles, and examined ontogenetic timing and volume of the otic capsule, oval window, operculum, opercularis muscle, columella (stapes), and extracolumella in three-dimensional histological reconstructions. All species had similar ontogenesis of the otic capsule, oval window, operculum, and opercularis muscle. Moreover, cell clusters of primordial columella in the oval window appeared just before metamorphosis in both eared and earless lineages. However, in earless lineages, the cell clusters either remained as small nubbins or cell buds in the location of the columella footplate within the oval window or disappeared by juvenile and adult stages. Thus, columella growth began around metamorphosis in all species but was truncated and/or degenerated after metamorphosis in earless species, leaving earless adults with morphology typical of metamorphic anurans. Shifts in the timing or expression of biochemical pathways that regulate the extension or differentiation of the columella after metamorphosis may be the developmental mechanism underlying convergent trait loss among toad lineages.

Conservation and divergence of YODA MAPKKK function in regulation of grass epidermal patterning.

All multicellular organisms must properly pattern cell types to generate functional tissues and organs. The organized and predictable cell lineages of the Brachypodium leaf enabled us to characterize the role of the MAPK kinase kinase gene BdYODA1 in regulating asymmetric cell divisions. We find that YODA genes promote normal stomatal spacing patterns in both Arabidopsis and Brachypodium, despite species-specific differences in those patterns. Using lineage tracing and cell fate markers, we show that, unexpectedly, patterning defects in bdyoda1 mutants do not arise from faulty physical asymmetry in cell divisions but rather from improper enforcement of alternative cellular fates after division. These cross-species comparisons allow us to refine our understanding of MAPK activities during plant asymmetric cell divisions.

The evolutionary origins of natural pedagogy: Rhesus monkeys show sustained attention following nonsocial cues versus social communicative signals.

The natural pedagogy hypothesis proposes that human infants preferentially attend to communicative signals from others, facilitating rapid cultural learning. In this view, sensitivity to such signals is a uniquely human adaptation and as such nonhuman animals should not produce or utilize these communicative signals. We test these evolutionary predictions by examining sensitivity to communicative cues in 206 rhesus monkeys (Macaca mulatta) using an expectancy looking time task modeled on prior work with infants. Monkeys observed a human actor who either made eye contact and vocalized to the monkey (social cue), or waved a fruit in front of her face and produced a tapping sound (nonsocial cue). The actor then either looked at an object (referential look) or looked toward empty space (look away). We found that, unlike human infants in analogous situations, rhesus monkeys looked longer at events following nonsocial cues, regardless of the demonstrator's subsequent looking behavior. Moreover younger and older monkeys showed similar patterns of responses across development. These results provide support for the natural pedagogy hypothesis, while also highlighting evolutionary changes in human sensitivity to communicative signals.

Conservation vs divergence in LEAFY and APETALA1 functions between Arabidopsis thaliana and Cardamine hirsuta.

A conserved genetic toolkit underlies the development of diverse floral forms among angiosperms. However, the degree of conservation vs divergence in the configuration of these gene regulatory networks is less clear. We addressed this question in a parallel genetic study between the closely related species Arabidopsis thaliana and Cardamine hirsuta. We identified leafy (lfy) and apetala1 (ap1) alleles in a mutant screen for floral regulators in C. hirsuta. C. hirsuta lfy mutants showed a complete homeotic conversion of flowers to leafy shoots, mimicking lfy ap1 double mutants in A. thaliana. Through genetic and molecular experiments, we showed that AP1 activation is fully dependent on LFY in C. hirsuta, by contrast to A. thaliana. Additionally, we found that LFY influences heteroblasty in C. hirsuta, such that loss or gain of LFY function affects its progression. Overexpression of UNUSUAL FLORAL ORGANS also alters C. hirsuta leaf shape in an LFY-dependent manner. We found that LFY and AP1 are conserved floral regulators that act nonredundantly in C. hirsuta, such that LFY has more obvious roles in floral and leaf development in C. hirsuta than in A. thaliana.

The genetic architecture of petal number in Cardamine hirsuta.

Invariant petal number is a characteristic of most flowers and is generally robust to genetic and environmental variation. We took advantage of the natural variation found in Cardamine hirsuta petal number to investigate the genetic basis of this trait in a case where robustness was lost during evolution. We used quantitative trait locus (QTL) analysis to characterize the genetic architecture of petal number. Αverage petal number showed transgressive variation from zero to four petals in five C. hirsuta mapping populations, and this variation was highly heritable. We detected 15 QTL at which allelic variation affected petal number. The effects of these QTL were relatively small in comparison with alleles induced by mutagenesis, suggesting that natural selection may act to maintain petal number within its variable range below four. Petal number showed a temporal trend during plant ageing, as did sepal trichome number, and multi-trait QTL analysis revealed that these age-dependent traits share a common genetic basis. Our results demonstrate that petal number is determined by many genes of small effect, some of which are age-dependent, and suggests a mechanism of trait evolution via the release of cryptic variation.

The Agricultural Origins of Time Preference.

This research explores the origins of observed differences in time preference across countries and regions. Exploiting a natural experiment associated with the expansion of suitable crops for cultivation in the course of the Columbian Exchange, the research establishes that pre-industrial agro-climatic characteristics that were conducive to higher return to agricultural investment, triggered selection, adaptation and learning processes that generated a persistent positive effect on the prevalence of long-term orientation in the contemporary era. Furthermore, the research establishes that these agro-climatic characteristics have had a culturally embodied impact on economic behavior such as technological adoption, education, saving, and smoking.

Cardamine hirsuta: a versatile genetic system for comparative studies.

A major goal in biology is to identify the genetic basis for phenotypic diversity. This goal underpins research in areas as diverse as evolutionary biology, plant breeding and human genetics. A limitation for this research is no longer the availability of sequence information but the development of functional genetic tools to understand the link between changes in sequence and phenotype. Here we describe Cardamine hirsuta, a close relative of the reference plant Arabidopsis thaliana, as an experimental system in which genetic and transgenic approaches can be deployed effectively for comparative studies. We present high-resolution genetic and cytogenetic maps for C. hirsuta and show that the genome structure of C. hirsuta closely resembles the eight chromosomes of the ancestral crucifer karyotype and provides a good reference point for comparative genome studies across the Brassicaceae. We compared morphological and physiological traits between C. hirsuta and A. thaliana and analysed natural variation in stamen number in which lateral stamen loss is a species characteristic of C. hirsuta. We constructed a set of recombinant inbred lines and detected eight quantitative trait loci that can explain stamen number variation in this population. We found clear phylogeographic structure to the genetic variation in C. hirsuta, thus providing a context within which to address questions about evolutionary changes that link genotype with phenotype and the environment.

A genetic perspective on glucose consumption in the cerebral cortex during human development.

As the major glucose-consuming organ in the human body, the dynamics of glucose metabolism in the brain deserve special attention. It has been shown that the brain's energy allocation as a percentage of the total energy budget of the individual peaks during childhood and declines through adolescence until reaching the stable allocation level seen in the adult. This pattern of glucose consumption has not been observed in other species, including our close primate relatives, and is therefore potentially either a driver or a consequence of human cognition. Furthermore, the allocation of glucose usage in the brain changes as the individual ages, with a surprising amount dedicated to glycolysis rather than oxidative phosphorylation pathway. This suggests that, at certain developmental stages, glucose-fuelled anabolic pathways, in addition to ATP generation, are the driving forces behind the brain's high energy requirement. In this study, we explore the most recent work pertaining to the dynamic glucose uptake and allocation of the developing human brain and investigate several genes that may play a role in regulating these processes.

Flexible information-seeking in chimpanzees.

Humans can flexibly use metacognition to monitor their own knowledge and strategically acquire new information when needed. While humans can deploy these skills across a variety of contexts, most evidence for metacognition in animals has focused on simple situations, such as seeking out information about the location of food. Here, we examine the flexibility, breadth, and limits of this skill in chimpanzees. We tested semi-free-ranging chimpanzees on a novel task where they could seek information by standing up to peer into different containers. In Study 1, we tested n = 47 chimpanzees to assess if chimpanzees would spontaneously engage in information-seeking without prior experience, as well as to characterize individual variation in this propensity. We found that many chimpanzees engaged in information-seeking with minimal experience, and that younger chimpanzees and females were more likely to do so. In two subsequent studies, we then further tested chimpanzees who initially showed robust information-seeking on new variations of this task, to disentangle the cognitive processing shaping their behaviors. In Study 2, we examined how a subset of n = 12 chimpanzees applied these skills to seek information about the location versus the identity of rewards, and found that chimpanzees were equally adept at seeking out location and identity information. In Study 3, we examined whether a subset of n = 6 chimpanzees could apply these skills to make more efficacious decisions when faced with uncertainty about reward payoffs. Chimpanzees were able to use information-seeking to resolve risk and choose more optimally when faced with uncertain payoffs, although they often also engaged in information-seeking when it was not strictly necessary. These results identify core features of flexible metacognition that chimpanzees share with humans, as well as constraints that may represent key evolutionary shifts in human cognition.

The Origins of Social Knowledge in Altricial Species.

Human infants are altricial, born relatively helpless and dependent on parental care for an extended period of time. This protracted time to maturity is typically regarded as a necessary epiphenomenon of evolving and developing large brains. We argue that extended altriciality is itself adaptive, as a prolonged necessity for parental care allows extensive social learning to take place. Human adults possess a suite of complex social skills, such as language, empathy, morality, and theory of mind. Rather than requiring hardwired, innate knowledge of social abilities, evolution has outsourced the necessary information to parents. Critical information for species-typical development, such as species recognition, may originate from adults rather than from genes, aided by underlying perceptual biases for attending to social stimuli and capacities for statistical learning of social actions. We draw on extensive comparative findings to illustrate that, across species, altriciality functions as an adaptation for social learning from caregivers.

Emerging Adulthood, a Pre-adult Life-History Stage.

The duration of human maturation has been underestimated; an additional 4-6-year pre-adult period of "emerging adulthood," should be included in models of human maturation. It is a period of brain maturation, learning about intimacy and mutual support, intensification of pre-existing friendships, family-oriented socialization, and the attainment of those social skills that are needed for mating and reproduction. We propose that emerging adulthood is a life-history stage that is a foundation of the high reproductive success of human beings. The period of emerging adulthood has an evolutionary context and developmental markers, and we present evidence that supports the idea that emerging adults require protection because they are still learning and maturing.

Leaf development and evolution.

Plant leaves are differentiated organs that arise sequentially from a population of pluripotent stem cells at the shoot apical meristem (SAM). There is substantial diversity in leaf shape, much of which depends on the size and arrangement of outgrowths at the leaf margin. These outgrowths are generated by a patterning mechanism similar to the phyllotactic processes producing organs at the SAM, which involves the transcription factors CUP-SHAPED COTYLEDON and the phytohormone auxin. In the leaf, this patterning mechanism creates sequential protrusions and indentations along the margin. The size, shape, and distribution of these protrusions also depend on the overall growth of the leaf lamina. Globally, growth is regulated by a complex genetic network controlling the distribution of cell proliferation and the timing of differentiation. Evolutionary changes in margin form arise from changes in two different classes of homeobox genes that modify the outcome of marginal patterning in diverse ways, and are under intense investigation.

The role of APETALA1 in petal number robustness.

Invariant floral forms are important for reproductive success and robust to natural perturbations. Petal number, for example, is invariant in Arabidopsis thaliana flowers. However, petal number varies in the closely related species Cardamine hirsuta, and the genetic basis for this difference between species is unknown. Here we show that divergence in the pleiotropic floral regulator APETALA1 (AP1) can account for the species-specific difference in petal number robustness. This large effect of AP1 is explained by epistatic interactions: A. thaliana AP1 confers robustness by masking the phenotypic expression of quantitative trait loci controlling petal number in C. hirsuta. We show that C. hirsuta AP1 fails to complement this function of A. thaliana AP1, conferring variable petal number, and that upstream regulatory regions of AP1 contribute to this divergence. Moreover, variable petal number is maintained in C. hirsuta despite sufficient standing genetic variation in natural accessions to produce plants with four-petalled flowers.

Tolerant Barbary macaques maintain juvenile levels of social attention in old age, but despotic rhesus macaques do not.

Complex social life is thought to be a major driver of complex cognition in primates, but few studies have directly tested the relationship between a given primate species' social system and their social cognitive skills. We experimentally compared life span patterns of a foundational social cognitive skill (following another's gaze) in tolerant Barbary macaques, Macaca sylvanus, and despotic rhesus macaques, Macaca mulatta. Semi-free-ranging monkeys (N = 80 individuals from each species) followed gaze more in test trials where an actor looked up compared to control trials. However, species differed in ontogenetic trajectories: both exhibited high rates of gaze following as juveniles, but rhesus monkeys exhibited declines in social attention with age, whereas Barbary macaques did not. This pattern indicates that developmental patterns of social attention vary with social tolerance, and that diversity in social behaviour can lead to differences in social cognition across primates.

Comparative Cuticle Development Reveals Taller Sporophytes Are Covered by Thicker Calyptra Cuticles in Mosses.

The calyptra is a maternal structure that protects the sporophyte offspring from dehydration, and positively impacts sporophyte survival and fitness in mosses. We explore the relationship between cuticle protection and sporophyte height as a proxy for dehydration stress in Funariaceae species with sporophytes across a range of sizes. Calyptrae and sporophytes from four species were collected from laboratory-grown populations at two developmental stages. Tissues were embedded, sectioned, and examined using transmission electron microscopy. Cuticle thickness was measured from three epidermal cells per organ for each individual and compared statistically. All four species have cuticles consisting of a cuticle proper and a cuticular layer on the calyptra and sporophyte at both developmental stages. Across species, shorter sporophytes are associated with smaller calyptra and thinner calyptra cuticles, whereas taller sporophytes are associated with larger calyptra and thicker calyptra cuticles. Independent of size, young sporophytes have a thin cuticle that thickens later during development, while calyptrae have a mature cuticle produced early during development that persists throughout development. This study adds to our knowledge of maternal effects influencing offspring survival in plants. Released from the pressures to invest in protection for their sporophyte offspring, maternal resources can be allocated to other processes that support sporophyte reproductive success. Using a comparative developmental framework enables us to broaden our understanding of cuticle development across species and provides structural evidence supporting the waterproofing role of the moss calyptra.