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Biology subjects

Zipple, M. N.

Publications and source records attributed to Zipple, M. N..

11 recordsLinked to original sources

Rewilding alters mouse epigenetic aging

The aging of mammalian epigenomes fundamentally alters cellular functions, and such changes are the focus of many healthspan and lifespan studies. However, studies of this process typically use mouse models living under standardized laboratory conditions and neglect the impact of variation in social, physical, microbial, and other aspects of the living environment on age-related changes. We examined differences in age-associated methylation changes between traditionally lab-reared and "rewilded" C57BL6/J mice, which lived in an outdoor field environment with enhanced ecological realism. Systematic analysis of age-associated methylation dynamics in the liver indicates a genomic region-conditioned, faster epigenetic aging rate in mice living in the field than those living in the lab, implicating perturbed 3D genome conformation and liver function. Altered epigenetic aging rates were more pronounced in sites that gain methylation with age, including sites enriched for transcription factor binding related to DNA repair. These observations underscore the overlooked role of the social and physical environment in epigenetic aging with implications for both basic and applied aging research.

genomics↗

Infant spatial relationships with adult males in a wild primate: males as mitigators or magnifiers of intergenerational effects of early adversity?

Adult male mammals can provide infants with protection and enhance their access to resources. They can also pose a risk to infants, either directly through infanticide or other aggression, or indirectly by placing infants at increased risk of conspecific or heterospecific conflict. Both benefits and costs may be especially important for offspring born to mothers in poor condition. Here we present the most detailed analysis to date of the influence of adult non-human primate males on a wide range of infant behaviors, and a description of the predictors of individual infants proximity to adult males. We show that the number of adult males near an infant predicts many infant behavioral traits, including aspects of the mother-infant relationship, infant activity budgets, and the frequency of social interactions with non-mothers. Infant exposure to adult males is statistically significantly repeatable over time (R = 0.16). This repeatability is partially explained by whether the infants mother experienced early life adversity: offspring of high-adversity mothers spent time in close proximity to more males during the first months of life. Our results are consistent with the possibility that the effects of maternal early life adversity can be mitigated or magnified by relationships with adult males.

ecology↗

Sex-specific competitive social feedback amplifies the role of early life contingency in male mice

Contingency (or luck) in early life plays an important role in shaping individuals development. When individuals live within larger societies, social experiences may cause the importance of early contingencies to be magnified or dampened. Here we test the hypothesis that competition magnifies the importance of early contingency in a sex-specific manner by comparing the developmental trajectories of genetically identical, free-living mice who either experienced high levels of territorial competition (males) or did not (females). We show that male territoriality results in a competitive feedback loop that magnifies the importance of early contingency and pushes individuals onto divergent, self-reinforcing life trajectories, while the same process appears absent in females. Our results indicate that the strength of sexual selection may be self-limiting, as within-sex competition increases the importance of early life contingency, thereby reducing the ability of selection to lead to evolution. They also demonstrate the potential for contingency to lead to dramatic differences in life outcomes, even in the absence of any underlying differences in ability ( merit).

evolutionary biology↗

Maternal Care Leads to the Evolution of Long, Slow Lives

Animals, and mammals in particular, vary widely in their "pace of life," with some species living long lives and reproducing infrequently (slow life histories) and others living short lives and reproducing often (fast life histories). These species also vary in the importance of maternal care in offspring fitness: in some species, offspring are fully independent of their mothers following a brief period of nutritional input, while others display a long period of continued dependence on mothers well after nutritional dependence. Here we hypothesize that these two axes of variation are causally related to each other, such that extended dependence of offspring on maternal presence leads to the evolution of longer lives at the expense of reproduction. We use a combination of deterministic modeling and stochastic agent-based modeling to explore how empirically-observed links between maternal survival and offspring fitness are likely to shape the evolution of mortality and fertility. Each of our modelling approaches leads to the same conclusion: when maternal survival has strong impacts on the survival of offspring and grandoffspring, populations evolve longer lives with less frequent reproduction. Our results suggest the slow life histories of humans and other primates as well as other long-lived, highly social animals such as hyenas, whales, and elephants, are partially the result of the strong maternal care that these animals display. We have designed our models to be readily parameterized with demographic data that is routinely collected by long-term researchers, which will facilitate more thorough testing of our hypothesis. Significance StatementHumans and other primates live longer lives and reproduce less often than other mammals of similar body mass. What is the cause of these long lives? Here we add to existing hypotheses, including the Mother and Grandmother hypotheses, by arguing that these increased lifespans are partially explained by the intense maternal care that many primates express. Using a combination of deterministic and stochastic modeling approaches, informed by empirical data, we show that stronger connections between maternal survival and offspring fitness leads to selection for longer lives and slower reproduction. Our models suggest that the importance of the mother-offspring relationship, which defines much of human and non-human primate lives, lies at the core of the evolution of our long lives.

evolutionary biology↗

Animal Emotions and Consciousness: Researchers' Perceptions, Biases, and Prospects for Future Progress

Do animals have emotions? Scientists and philosophers have long struggled with this question, with debates ranging from whether animals experience an "internal world" to whether we are capable of studying it. Recently, theoretical, and methodological advances have rekindled this debate, yet, it is unclear where the scientific consensus on these topics lies today. To address this gap, we administered a survey of professional animal behavior researchers to assess perceptions regarding (1) the taxonomic distribution of emotions and consciousness in non-human animals, (2) respondents confidence in this assessment, and (3) attitudes towards potential for progress and possible pitfalls when addressing these questions. In general, animal behavior researchers (n=100) ascribed emotionality and consciousness to a broad swath of the animal taxa, including non-human primates, other mammals, birds, and cephalopods, with varying degrees of confidence. There was a strong positive relationship between how likely a respondent was to attribute emotions to a given taxa and their confidence in that assessment, with respondents assuming an absence of emotions and consciousness when they were unsure. In addition, respondents assessments were shaped by several traits (e.g., advanced cognitive abilities, consciousness) that they also admitted were not necessary for an animal to experience emotions. Ultimately, a large majority of researchers were optimistic that tools either currently exist or will exist in the future to rigorously address these questions (>85%) and that animal behavior, as a field, should do more to encourage emotions research (71%). We discuss implications of our findings for publication bias, ethical considerations, and identify an emergent consensus for the need of a functional definition of emotions to facilitate future work. Significance StatementEmotions and consciousness are fundamental components of human experience--these phenomena are central to our behavior, relationships, and sense of meaning. Whether these experiences are shared by non-human animals has long been a subject of philosophical and scientific debate. In this paper we describe, for the first time, results from a survey of animal behavior researchers regarding their perceptions of these questions and the ability of science to answer them. Researchers ascribe emotions and consciousness to many taxa, and their likelihood of doing was strongly predicted by phylogeny and researchers confidence in their answers. We hope these results spur additional interdisciplinary collaboration to rigorously pursue these questions and create a baseline for future comparisons to track scientific attitudes over time. O_QD"I have chosen bats instead of wasps or flounders because if one travels too far down the phylogenetic tree, people gradually shed their faith that there is experience there at all"--Thomas Nagel C_QD

animal behavior and cognition↗

Genetically Identical Mice Express Alternative Reproductive Tactics Depending on Social Conditions in the Field

In many species, establishing and maintaining a territory is critical to survival and reproduction, and an animals ability to do so is strongly influenced by the presence and density of competitors. Here we manipulate social conditions to study the alternative reproductive tactics displayed by genetically identical, age-matched laboratory mice competing for territories under ecologically realistic social environmental conditions. We introduced adult males and females of the laboratory mouse strain (C57BL/6J) into a large, outdoor field enclosure containing defendable resource zones under one of two social conditions. We first created a low-density social environment, such that the number of available territories exceeded the number of males. After males established stable territories, we introduced a pulse of intruder males and observed the resulting defensive and invasive tactics employed. In response to this change in social environment, males with large territories invested more in patrolling but were less effective at excluding intruder males as compared to males with small territories. Intruding males failed to establish territories and displayed an alternative tactic featuring greater exploration as compared to genetically identical territorial males. Alternative tactics did not lead to equal reproductive success--males that acquired territories experienced greater survival and had greater access to females.

ecology↗

Five decades of data yield no support for adaptive biasing of offspring sex ratio in wild baboons (Papio cynocephalus)

Over the past 50 years, a wealth of testable, often conflicting, hypotheses have been generated about the evolution of offspring sex ratio manipulation by mothers. Several of these hypotheses have received support in studies of invertebrates and some vertebrate taxa. However, their success in explaining sex ratios in mammalian taxa, and especially in primates, has been mixed. Here, we assess the predictions of four different hypotheses about the evolution of biased offspring sex ratios in the well-studied baboons of the Amboseli basin in Kenya: the Trivers-Willard, female rank enhancement, local resource competition, and local resource enhancement hypotheses. Using the largest sample size ever analyzed in a primate population (n = 1372 offspring), we test the predictions of each hypothesis. Overall, we find no support for adaptive biasing of sex ratios. Offspring sex is not consistently related to maternal dominance rank or biased towards the dispersing sex, nor it is predicted by group size, population growth rates, or their interaction with maternal rank. Because our sample size confers power to detect even subtle biases in sex ratio, including modulation by environmental heterogeneity, these results suggest that adaptive biasing of offspring sex does not occur in this population.

evolutionary biology↗

Beyond orphaned infants: novel effects of maternal death in wild primates

Primate offspring often depend on their mothers well beyond the age of weaning, and offspring that experience maternal death in early life can suffer substantial reductions in fitness across the lifespan. Here we leverage data from eight wild primate populations (seven species) to examine two underappreciated pathways linking early maternal death and offspring fitness that are distinct from direct effects of orphaning on offspring survival. First, we show that, for five of the seven species, offspring face reduced survival during the years immediately preceding maternal death, while the mother is still alive. Second, we identify an intergenerational effect of early maternal loss in three species (muriquis, baboons, and blue monkeys), such that early maternal death experienced in one generation leads to reduced offspring survival in the next. Our results have important implications for the evolution of slow life histories in primates, as they suggest that maternal condition and survival are more important for offspring fitness than previously realized.

evolutionary biology↗

Threshold assessment, categorical perception, and the evolution of reliable signaling

Animals often use assessment signals to communicate information about their quality to a variety of receivers, including potential mates, competitors, and predators. But what maintains reliable signaling and prevents signalers from signaling a better quality than they actually have? Previous work has shown that reliable signaling can be maintained if signalers pay fitness costs for signaling at different intensities and these costs are greater for lower quality individuals than higher quality ones. Models supporting this idea typically assume that continuous variation in signal intensity is perceived as such by receivers. In many organisms, however, receivers have threshold responses to signals, in which they respond to a signal if it is above a threshold value and do not respond if the signal is below the threshold value. Here, we use both analytical and individual-based models to investigate how such threshold responses affect the reliability of assessment signals. We show that reliable signaling systems can break down when receivers have an invariant threshold response, but reliable signaling can be rescued if there is variation among receivers in the location of their threshold boundary. Our models provide an important step towards understanding signal evolution when receivers have threshold responses to continuous signal variation.

animal behavior and cognition↗

Comparing proportional and ordinal dominance ranks reveals multiple competitive landscapes in an animal society

Across group-living animals, linear dominance hierarchies lead to disparities in access to resources, health outcomes, and reproductive performance. Studies of how dominance rank affects these outcomes typically employ one of several dominance rank metrics without examining the assumptions each metric makes about its underlying competitive processes. Here we compare the ability of two dominance rank metrics--ordinal rank and proportional or standardized rank--to predict 20 distinct traits in a well-studied wild baboon population in Amboseli, Kenya. We propose that ordinal rank best predicts outcomes when competition is density-dependent, while proportional rank best predicts outcomes when competition is density-independent. We found that for 75% (15/20) of the traits, one of the two rank metrics performed better than the other. Strikingly, all male traits were better predicted by ordinal than by proportional rank, while female traits were evenly split between being better predicted by proportional or ordinal rank. Hence, male and female traits are shaped by different competitive regimes: males competitive environments are largely driven by density-dependent resource access (e.g., access to estrus females), while females competitive environments are shaped by both density-independent resource access (e.g. distributed food resources) and density-dependent resource access. However, traits related to competition for social and mating partners are an exception to this sex-biased pattern: these traits were better predicted by ordinal rank than by proportional rank for both sexes. We argue that this method of comparing how different rank metrics predict traits of interest can be used as a way to distinguish between different competitive processes operating in animal societies.

animal behavior and cognition↗

Intergenerational effects of early adversity on survival in wild baboons

In humans and nonhuman animals, early life adversity can affect an individuals health, survival, and fertility for many years after the adverse experience. However, whether early life adversity also imposes intergenerational effects on the exposed individuals offspring is not well understood. Here, we fill this gap by leveraging prospective, longitudinal data on a wild, long-lived primate. We find that juveniles whose mothers experienced early life adversity exhibit high mortality before age 4, and this effect is independent of the juveniles own experience of early adversity. Furthermore, our results point towards a strong role for classic parental effects in driving these effects: mothers that experienced early life adversity displayed reduced viability in adulthood, which in turn led to reductions in offspring survival. Importantly, these mothers juvenile offspring often preceded them in death by 1 to 2 years, indicating that, for high adversity mothers, the quality of maternal care declines near the end of life. While we cannot exclude direct effects of a parents environment on offspring quality (e.g., transgenerational epigenetic changes), our results are most consistent with a classic parental effect, in which the environment experienced by a parent affects its future phenotype and therefore its offsprings phenotype. Together, our findings demonstrate that adversity experienced by individuals in one generation can have strong effects on the survival of offspring in the next generation, even if those offspring did not themselves experience early adversity.

zoology↗