New York Consortium in Evolutionary Primatology

Societal Impact Statement Soils are globally degraded due in part to conventional agriculture and wildland conversion. To address the global challenge of soil degradation, we formed an interdisciplinary, cross‐institutional collaborative research team, New Roots for Restoration, to understand how perennial plant root and shoot traits relate to one another, and how they influence and are influenced by plant communities and the soil. We highlight how coordinated research projects, expertise cores, and cross‐institution training activities simultaneously advance scientific understanding and workforce development. We share approaches and tools, as well as challenges and lessons learned. This institute highlights how multi‐institution teams integrating diverse biological subdisciplines can advance major scientific and training goals. Summary The challenge of restoring degraded soils must be met with integrated knowledge and practice of distinct biological subdisciplines. Here we share a model of scientific collaboration, an interdisciplinary cross‐institution team: New Roots for Restoration Biology Integration Institute (NRR). NRR focuses on how plant organismal systems (roots and shoots) relate to one another, and how those relationships influence and are influenced by plant communities and the soil ecosphere. Our aim is to enhance the ability to predict belowground functional traits from aboveground phenotypes to identify ecologically and functionally appropriate materials to restore natural ecosystems and to develop sustainable agricultural systems of the future. Plants provide the ecological and structural foundation of terrestrial landscapes, building soils and supporting productivity in natural and agricultural ecosystems. Plants connect aboveground components through their root systems in terrestrial ecosystems to the soil ecosphere. However, the field lacks a basic understanding of how plant traits, from roots to shoots, govern these connections. This is especially true for perennial plants, which are inherently difficult to study. NRR seeks to elucidate how attributes of the plant organismal system (plant traits, genetics, genetics × environment interactions), community ecology, and the soil ecosphere contribute to variation in aboveground and belowground plant structures through 10 integrated projects supported by expertise cores. Our efforts demonstrate how the integration of biological subdisciplines can advance understanding of the impacts of deep‐rooted plant systems in both restored grasslands and perennial agroecosystems.

Extrinsic postzygotic isolation, where hybrids experience reductions in fitness due to a mismatch with their environment, is central to speciation. Knowledge of genetic variants that underlie extrinsic isolation is crucial for understanding the early stages of speciation. Differences in seasonal migration are strong candidates for extrinsic isolation (e.g., if hybrids take intermediate and inferior routes compared to pure forms). Here, we used a hybrid zone between two subspecies of the songbird Swainson's thrush (Catharus ustulatus) with different migratory routes and tests for viability selection (locus-specific changes in interspecific heterozygosity and ancestry mismatch across age classes) to gain insight into the genetic basis of extrinsic isolation. Using data from over 900 individuals we find strong evidence for viability selection on both interspecific heterozygosity and ancestry mismatch at loci linked to migration. Much of this selection was dependent on genome-wide ancestry; as expected, a subset of hybrids exhibited reduced viability, but remarkably, another subset appears to fill an unoccupied fitness peak within the species, exhibiting higher viability than even parental forms. Many of the variants that influence hybrid viability appear to occur in structural variants, including a putative pericentric inversion. Our study emphasizes the importance of epistatic interactions and structural variants in speciation.

Age and early life adversity (ELA) are both key determinants of health, but whether they target similar physiological mechanisms across the body is unknown due to limited multi-tissue datasets from well-characterized cohorts. We generated DNA methylation (DNAm) profiles across 14 tissues in 237 semi-free ranging rhesus macaques, with records of naturally occurring ELA. We show that age-associated DNAm variation is predominantly tissue-dependent, yet tissue-specific epigenetic clocks reveal that the pace of epigenetic aging is relatively consistent within individuals. ELA effects on loci are adversity-dependent, but a given ELA has a coordinated impact across tissues. Finally, ELA targeted many of the same loci as age, but the direction of these effects varied, indicating that ELA does not uniformly contribute to accelerated age in the epigenome. ELA thus imprints a coordinated, tissue-spanning epigenetic signature that is both distinct from and intertwined with age-related change, advancing our understanding of how early environments sculpt the molecular foundations of aging and disease.

The effect of the social environment on the proinflammatory immune response may mediate the relationship between social environment and fitness but remains understudied outside captive animals and human populations. Age can also influence both immune function and social behaviour, and hence may modulate their relationships. This study investigates the role of social interactions in driving the concentrations of two urinary markers of proinflammatory immune activation, neopterin and soluble urokinase plasminogen activator receptor (suPAR), in a free-ranging population of rhesus macaques, Macaca mulatta. We collected 854 urine samples from 172 adult monkeys and quantified how urinary suPAR and neopterin concentrations were related to affiliative behaviour and agonistic behaviour received over 60 days. In females, but not in males, higher rates of affiliative interactions were associated with lower neopterin concentrations, while conversely, experiencing more agonistic interactions was associated with higher neopterin concentrations. The association between affiliation and neopterin concentration was modulated by age, with older females experiencing a stronger negative association between affiliative behaviour and neopterin concentration. There were no associations between suPAR concentration and social environment for either sex. This study demonstrates that proinflammatory immune activity is a potential mechanism mediating the association between social environment and fitness under naturalistic conditions and that age can be an important modulator of the effect of social environment on the immune system.

Pathologies of the skull and teeth are well documented for many human populations, but there are fewer studies of other primates. We contrast lesion prevalence and patterning among cercopithecoid primates and map variation onto socioecological variables. We compare craniodental lesions in six species: Nasalis larvatus (n = 54), Colobus polykomos (n = 64), Cercopithecus mitis (n = 65), Macaca fascicularis (n = 109), Theropithecus gelada (n = 13), and Papio anubis (n = 76). One of us (C.A.K.) evaluated each adult skull for multiple lesion types using standard criteria. We also tested for a relationship between lesion prevalence and cranial suture fusion (age proxy). We used nonparametric tests for sex and species differences as well as pathology co-occurrence in SPSS. Socioecological data come from previous studies. Sex differences in lesion prevalence were only detected in P. anubis. Within taxa, some lesion types co-occurred. In Macaca, the presence of caries was associated with several other lesion types. Pulp cavity exposure co-occurred with TMJ osteoarthritis in multiple taxa. Among taxa, male P. anubis had higher lesion prevalences, particularly related to the anterior dentition and facial trauma. Because we did not detect a relationship between suture fusion and lesion prevalence, we propose that craniodental lesions may also be influenced by socioecological variables such as group composition and ratio of fruit to leaves in the diet. Our findings suggest that pain from pulp cavity exposure and related dental infections may alter chewing biomechanics and contribute to onset of TMJ osteoarthritis in nonhuman primates, as seen in humans. Further, we suggest that higher lesion prevalence in male baboons is likely related to male-male competition. Skeletal lesion analysis provides useful insight into primate socioecology, particularly for rare or difficult-to-observe phenomena, and provides additional biological context for our own species.

The mammalian inner ear contains the sensory organs responsible for balance (semicircular canals, utricle, and saccule) and hearing (cochlea). While these organs are functionally distinct, there exists a critical structural connection between the two: the ductus reuniens (DR). Despite its functional importance, comparative descriptions of DR morphology are limited, hindering our understanding of the evolutionary diversification of hearing and balance systems among mammals. Using virtual 3D models derived from micro-CT, we examine the morphology of the DR and its relationship to the bony labyrinth in humans compared to that in a commonly used animal model, the guinea pig. Anatomical reconstructions and univariate measurements were carried out in the software 3D Slicer. Data indicate similarities in DR morphology between humans and guinea pigs in terms of overall shape. However, there are considerable differences in relative DR length and width between humans and guinea pigs. Humans possess a relatively shorter and narrower DR but with wider openings to the saccule and cochlear duct. This results in a relatively more constricted DR lumen in humans which may differentially limit fluid transfer between the saccule and cochlea. Our results reveal previously hidden morphological diversity in the communication between the hearing and balance systems of the mammalian inner ear which may indicate alternative strategies for isolating the Organ of Corti from the peripheral vestibular system throughout mammalian evolution.

Data sharing notapplicable to this article as no datasets were generated or analysed during thecurrent study.

The evolutionary history of canids and felids is marked by a deep time separation that has uniquely shaped their behavior and phenotype toward refined predatory abilities. The caudate nucleus is a subcortical brain structure associated with both motor control and cognitive, emotional, and executive functions. We used a combination of three-dimensional imaging, allometric scaling, and structural analyses to compare the size and shape characteristics of the caudate nucleus. The sample consisted of MRI scan data obtained from six canid species (Canis lupus lupus, Canis latrans, Chrysocyon brachyurus, Lycaon pictus, Vulpes vulpes, Vulpes zerda), two canid subspecies (Canis lupus familiaris, Canis lupus dingo), as well as three felids (Panthera tigris, Panthera uncia, Felis silvestris catus). Results revealed marked conservation in the scaling and shape attributes of the caudate nucleus across species, with only slight deviations. We hypothesize that observed differences in caudate nucleus size and structure for the domestic canids are reflective of enhanced cognitive and emotional pathways that possibly emerged during domestication.

Estimation of body mass from skeletal metrics can reveal important insights into the paleobiology of archeological or fossil remains. The standard approach constructs predictive equations from postcrania, but studies have questioned the reliability of traditional measures. Here, we examine several skeletal features to assess their accuracy in predicting body mass. Antemortem mass measurements were compared with common skeletal dimensions from the same animals postmortem, using 115 rhesus macaques (male: n = 43; female: n = 72). Individuals were divided into training (n = 58) and test samples (n = 57) to build and assess Ordinary Least Squares or multivariate regressions by residual sum of squares (RSS) and AIC weights. A leave-one-out approach was implemented to formulate the best fit multivariate models, which were compared against a univariate and a previously published catarrhine body-mass estimation model. Femur circumference represented the best univariate model. The best model overall was composed of four variables (femur, tibia and fibula circumference and humerus length). By RSS and AICw, models built from rhesus macaque data (RSS = 26.91, AIC = -20.66) better predicted body mass than did the catarrhine model (RSS = 65.47, AIC = 20.24). Body mass in rhesus macaques is best predicted by a 4-variable equation composed of humerus length and hind limb midshaft circumferences. Comparison of models built from the macaque versus the catarrhine data highlight the importance of taxonomic specificity in predicting body mass. This paper provides a valuable dataset of combined somatic and skeletal data in a primate, which can be used to build body mass equations for fragmentary fossil evidence.