Sex-specific innate immunity and ageing in long-lived fresh water turtles (Kinosternon flavescens: Kinosternidae).

BACKGROUND: The progressive deregulation of the immune system with age, termed immunosenescence, has been well studied in mammalian systems, but studies of immune function in long-lived, wild, non-mammalian populations are scarce. In this study we leverage a 38-year mark-recapture study to quantify the relationships among age, sex, survival, reproductive output and the innate immune system in a long-lived reptile, yellow mud turtles (Kinosternon flavescens; Testudines; Kinosternidae). METHODS: We estimated rates of survival and age-specific mortality by sex based on mark-recapture data for 1530 adult females and 860 adult males over 38 years of captures. We analyzed bactericidal competence (BC), and two immune responses to foreign red blood cells - natural antibody-mediated haemagglutination (NAbs), and complement-mediated haemolysis ability (Lys) - in 200 adults (102 females; 98 males) that ranged from 7 to 58 years of age captured in May 2018 during their emergence from brumation, and for which reproductive output and long-term mark-recapture data were available. RESULTS: We found that females are smaller and live longer than males in this population, but the rate of accelerating mortality across adulthood is the same for both sexes. In contrast, males exhibited higher innate immunity than females for all three immune variables we measured. All immune responses also varied inversely with age, indicating immunosenescence. For females that reproduced in the preceding reproductive season, egg mass (and therefore total clutch mass) increased with age,. In addition to immunosenescence of bactericidal competence, females that produced smaller clutches also had lower bactericidal competence. CONCLUSIONS: Contrary to the general vertebrate pattern of lower immune responses in males than females (possibly reflecting the suppressive effects of androgens), we found higher levels of all three immune variables in males. In addition, contrary to previous work that found no evidence of immunosenescence in painted turtles or red-eared slider turtles, we found a decrease in bactericidal competence, lysis ability, and natural antibodies with age in yellow mud turtles.

Maternal allocation of carotenoids to eggs in an Anolis lizard.

The maternal allocation of carotenoids to eggs has been widely documented and manipulated. However, it is often assumed that the sole adaptive value of this allocation is to increase offspring fitness. Because carotenoids can be pro-oxidants or antioxidants depending on their concentrations and their chemical environment (i.e. presence of other antioxidants), dams may need to dispose of excess carotenoids upon depletion of other antioxidants to prevent oxidative damage. Additionally, the amount of carotenoids deposited in eggs may be dependent on male traits such as quality and coloration. We evaluated these two non-mutually exclusive hypotheses for carotenoid allocation to eggs and assessed paternal effects by supplementing male and female brown anole lizards, Anolis sagrei, with dietary carotenoids or with a combination of carotenoids and vitamin C. We found significant differences in the antioxidant capacities of fertilized and unfertilized eggs produced by female lizards, but the treatment did not affect the antioxidant capacity or carotenoid content of eggs. However, the carotenoid concentration of unfertilized eggs from carotenoid-supplemented females was significantly higher than eggs from the control group. Male coloration and body size did not affect the antioxidant capacity or carotenoid content of the eggs. Carotenoids may be allocated to unfertilized eggs to offset oxidative damage to the dam, with a neutral effect on offspring, rather than to solely provide antioxidant benefits to offspring as has been widely assumed.

Evaluating the interactive effects of artificial light at night and background color on tadpole crypsis, background adaptation efficacy, and growth.

Artificial light at night (ALAN) is a global pollutant of rising concern. While alterations to natural day-night cycles caused by ALAN can affect a variety of traits, the broader fitness and ecological implications of these ALAN-induced shifts remain unclear. This study evaluated the interactive effects of ALAN and background color on traits that have important implications for predator-prey interactions and fitness: crypsis, background adaptation efficacy, and growth. Using three amphibian species as our models, we discovered that: (1) Exposure to ALAN reduced the ability for some species to match their backgrounds (background adaptation efficacy), (2) Crypsis and background adaptation efficacy were enhanced when tadpoles were exposed to dark backgrounds only, emphasizing the importance of environmental context when evaluating the effects of ALAN, (3) ALAN and background color have a combined effect on a common metric of fitness (growth), and (4) Effects of ALAN were not generalizable across amphibian species, supporting calls for more studies that utilize a diversity of species. Notably, to our knowledge, we found the first evidence that ALAN can diminish background adaptation efficacy in an amphibian species (American toad tadpoles). Collectively, our study joins others in highlighting the complex effects of ALAN on wildlife and underscores the challenges of generalizing ALAN's effect across species, emphasizing the need for a greater diversity of species and approaches used in ALAN research.

The morphological effects of artificial light at night on amphibian predators and prey are masked at the community level.

Artificial light at night (ALAN) is a pervasive pollutant that influences wildlife at both the individual and community level. In this study, we tested the individual-level effects of ALAN on three species of tadpole prey and their newt predators by measuring prey pigmentation and predator and prey mass. Then we evaluated whether the individual-level effects of ALAN on pigmentation and mass had cascading community-level effects by assessing the outcome of predator-prey interactions. We found that spring peepers exposed to ALAN were significantly darker than those reared under control conditions. Additionally, wood frogs reared in ALAN conditions were significantly smaller than those reared in control conditions. In contrast, Eastern newts collected earlier in the spring that were exposed to ALAN were significantly larger than controls while those collected later in the spring were not affected by ALAN, suggesting phenological differences in the effect of ALAN. To understand how changes in pigmentation and size due to ALAN influence predation rates, we ran predation assays in both ALAN-polluted and ALAN-free outdoor environments. After the predation assay, the size disparity in wood frogs reared in ALAN was eliminated such that there was no longer a treatment difference in wood frog size, likely due to size-selective predation. This demonstrates the beneficial nature of predators' selective pressure on prey populations. Lastly, despite individual-level effects of ALAN on pigmentation and mass, we did not detect cascading community-level effects on predation rates. Overall, this study highlights important species-level distinctions in the effects of ALAN. It also emphasizes the need to incorporate ecological complexity to understand the net impact of ALAN.

A Framework for Investigating Rules of Life by Establishing Zones of Influence.

The incredible complexity of biological processes across temporal and spatial scales hampers defining common underlying mechanisms driving the patterns of life. However, recent advances in sequencing, big data analysis, machine learning, and molecular dynamics simulation have renewed the hope and urgency of finding potential hidden rules of life. There currently exists no framework to develop such synoptic investigations. Some efforts aim to identify unifying rules of life across hierarchical levels of time, space, and biological organization, but not all phenomena occur across all the levels of these hierarchies. Instead of identifying the same parameters and rules across levels, we posit that each level of a temporal and spatial scale and each level of biological organization has unique parameters and rules that may or may not predict outcomes in neighboring levels. We define this neighborhood, or the set of levels, across which a rule functions as the zone of influence. Here, we introduce the zone of influence framework and explain using three examples: (a) randomness in biology, where we use a Poisson process to describe processes from protein dynamics to DNA mutations to gene expressions, (b) island biogeography, and (c) animal coloration. The zone of influence framework may enable researchers to identify which levels are worth investigating for a particular phenomenon and reframe the narrative of searching for a unifying rule of life to the investigation of how, when, and where various rules of life operate.

Sex-related differences in aging rate are associated with sex chromosome system in amphibians.

Sex-related differences in mortality are widespread in the animal kingdom. Although studies have shown that sex determination systems might drive lifespan evolution, sex chromosome influence on aging rates have not been investigated so far, likely due to an apparent lack of demographic data from clades including both XY (with heterogametic males) and ZW (heterogametic females) systems. Taking advantage of a unique collection of capture-recapture datasets in amphibians, a vertebrate group where XY and ZW systems have repeatedly evolved over the past 200 million years, we examined whether sex heterogamy can predict sex differences in aging rates and lifespans. We showed that the strength and direction of sex differences in aging rates (and not lifespan) differ between XY and ZW systems. Sex-specific variation in aging rates was moderate within each system, but aging rates tended to be consistently higher in the heterogametic sex. This led to small but detectable effects of sex chromosome system on sex differences in aging rates in our models. Although preliminary, our results suggest that exposed recessive deleterious mutations on the X/Z chromosome (the "unguarded X/Z effect") or repeat-rich Y/W chromosome (the "toxic Y/W effect") could accelerate aging in the heterogametic sex in some vertebrate clades.

Diverse aging rates in ectothermic tetrapods provide insights for the evolution of aging and longevity.

Comparative studies of mortality in the wild are necessary to understand the evolution of aging; yet, ectothermic tetrapods are underrepresented in this comparative landscape, despite their suitability for testing evolutionary hypotheses. We present a study of aging rates and longevity across wild tetrapod ectotherms, using data from 107 populations (77 species) of nonavian reptiles and amphibians. We test hypotheses of how thermoregulatory mode, environmental temperature, protective phenotypes, and pace of life history contribute to demographic aging. Controlling for phylogeny and body size, ectotherms display a higher diversity of aging rates compared with endotherms and include phylogenetically widespread evidence of negligible aging. Protective phenotypes and life-history strategies further explain macroevolutionary patterns of aging. Analyzing ectothermic tetrapods in a comparative context enhances our understanding of the evolution of aging.

Trade-offs between reproductive coloration and innate immunity in a natural population of female sagebrush lizards, Sceloporus graciosus.

Trade-offs between immune function and reproduction are common to many organisms. Nevertheless, high energetic resources may eliminate the need for these trade-offs. In this study, we consider the effects of food availability on these trade-offs in a wild population of female sagebrush lizards (Sceloporus graciosus) during the breeding season. We manipulated food availability by supplementing some lizards but not others. We measured female orange side coloration as an indicator of reproductive state and calculated the bacterial killing capability of collected plasma exposed to Escherichia coli ex vivo as a measure of innate immunity. We found that female lizards show a natural trade-off between reproductive effort and immune function; females under high reproductive investment had lower innate immunity than those at a later reproductive state. We did not detect this trade-off with food supplementation. We show that trade-offs depend on the energetic state of the animal, illustrating that trade-offs between immune function and reproduction can be context-dependent.

Expanding the landscape of opportunity: Professional societies support early-career researchers through community programming and peer coaching.

Weaving the future of the field of comparative psychology is dependent on the career advancement of early-career scientists. Despite concerted efforts to increase diversity in science, technology, engineering, and mathematics, scholars from marginalized groups are disproportionately underrepresented in the field-especially at advanced career stages. New approaches to sponsorship, mentoring, and community building are necessary to retain talent from marginalized communities and to create a culture and a system where all individuals can thrive. We describe the unique and supportive role of senior women scientists united through a professional society in initiating peer coaching circles to facilitate the success of a diverse cohort of early-career women scientists. We offer our experiences with the Weaving the Future of Animal Behavior program as a case study that illustrates the cascading impacts of professional societies investing in the success and career development of marginalized scholars. We focus on our peer coaching circle experience and share the products and outcomes after 2 years of meeting. Peer coaching transformed us from a group of loosely organized, anxious individuals into a collective of empowered agents of change with an enhanced sense of belonging. We end by presenting recommendations to institutions seeking to expand the landscape of opportunities to other marginalized scholars. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Joint estimation of growth and survival from mark-recapture data to improve estimates of senescence in wild populations.

Understanding age-dependent patterns of survival is fundamental to predicting population dynamics, understanding selective pressures, and estimating rates of senescence. However, quantifying age-specific survival in wild populations poses significant logistical and statistical challenges. Recent work has helped to alleviate these constraints by demonstrating that age-specific survival can be estimated using mark-recapture data even when age is unknown for all or some individuals. However, previous approaches do not incorporate auxiliary information that can improve age estimates of individuals. We introduce a survival estimator that combines a von Bertalanffy growth model, age-specific hazard functions, and a Cormack-Jolly-Seber mark-recapture model into a single hierarchical framework. This approach allows us to obtain information about age and its uncertainty based on size and growth for individuals of unknown age when estimating age-specific survival. Using both simulated and real-world data for two painted turtle (Chrysemys picta) populations, we demonstrate that this additional information substantially reduces the bias of age-specific hazard rates, which allows for the testing of hypotheses related to aging. Estimating patterns of senescence is just one practical application of jointly estimating survival and growth; other applications include obtaining better estimates of the timing of recruitment and improved understanding of life-history trade-offs between growth and survival.

A novel body coloration phenotype in Anolis sagrei: Implications for physiology, fitness, and predation.

In animals, color signals that convey information about quality are often associated with costs linked to the expression of coloration and may therefore be honest signals of sender quality. Honest indicators are often seen in sexual signals that are used by males to advertise quality to females. Carotenoid and pterin pigments are responsible for yellow, orange, and red coloration in a variety of taxa, but can also serve important roles as antioxidants by reducing free radicals in the body. In this study, we test the effects of a novel full-bodied orange color phenotype of the brown anole, Anolis sagrei, on mate choice, physiology, and survival. We found no evidence that lizards expressing the orange phenotype were preferred by females. Additionally, they did not differ in immune function, running endurance, or maximum sprint speed from lizards that did not express the novel phenotype. Pigment extractions revealed that orange body coloration resulted from pterin pigments and not carotenoids. Visual models suggest that the orange phenotype is less conspicuous to bird predators than the brown phenotype and may provide an adaptive explanation for the persistence of this trait. Given its small, yet positive effect on fitness, we expect the orange color phenotype to increase in frequency in subsequent decades.