The Conundrum of Heterogeneities in Life History Studies Cam, Emmanuelle; Aubry, Lise M.; Authier, Matthieu
Trends in ecology & evolution (Amsterdam),
November 2016, 2016-11-00, 20161101, Letnik:
31, Številka:
11
Journal Article
Recenzirano
What causes interindividual variation in fitness? Evidence of heritability of latent individual fitness traits has resparked a debate about the causes of variation in life histories in populations: ...neutralism versus empirical adaptationism. This debate about the processes underlying observed variation pits neutral stochastic demographic processes against evolutionarily relevant differences among individual fitness traits. Advancing this debate requires careful consideration of differences among inference approaches used by proponents of each hypothesis. Here we draw parallels between several disciplines focusing on processes generating variation in individuals’ life-course, and we contrast methodologies to disentangle these processes. We draw on other disciplines to clarify terminology, risks of flawed inference, and expand the panel of hypotheses and formalizations of processes generating variation in life histories.
Evidence of heritability of individual fitness traits in wild populations has reopened a debate about the relative contribution of neutral, stochastic demographic processes to observed variations in life histories.
There are conceptual differences among published studies documenting heterogeneity in life histories; differences so fundamental that they led to misunderstandings between schools of thought.
The question of the processes generating heterogeneity in longitudinal trajectories has stimulated a large body of work in econometrics, political, social and biomedical sciences, which have highlighted risks of flawed inference; these risks have been overlooked in biology.
Other disciplines offer useful frameworks for future work on life histories in three areas: terminology, the characterization of the diversity of processes underlying variation in life histories, and the methods of statistical inference to disentangle these processes.
We surveyed ecologists and evolutionary biologists in American universities to understand how they are coping with the COVID-19 pandemic. Female respondents, assistant professors, and those who care ...for at least one child or teenager, were significantly more dissatisfied with their work–life balance during this pandemic than others, and further expected these negative impacts to be long lived. Online teaching support, relaxed expectations on publications, the possibility of pausing the tenure clock, and an acknowledgment of “no business as usual” by administrators were thought to be effective policies in mitigating these negative impacts. This survey serves as a manifesto to what our professional community is currently experiencing, and should be used to inform academic policies directed at improving faculty productivity and welfare.
1. Individuals are heterogeneous in many ways. Some of these differences are incorporated as individual states (e.g. age, size, breeding status) in population models. However, substantial amounts of ...heterogeneity may remain unaccounted for, due to unmeasurable genetic, maternal or environmental factors. 2. Such unobserved heterogeneity (UH) affects the behaviour of heterogeneous cohorts via intra-cohort selection and contributes to inter-individual variance in demographic outcomes such as longevity and lifetime reproduction. Variance is also produced by individual stochasticity, due to random events in the life cycle of wild organisms, yet no study thus far has attempted to decompose the variance in demographic outcomes into contributions from UH and individual stochasticity for an animal population in the wild. 3. We developed a stage-classified matrix population model for the southern fulmar breeding on lle des Pétrels, Antarctica. We applied multievent, multistate mark-recapture methods to estimate a finite mixture model accounting for UH in all vital rates and Markov chain methods to calculate demographic outcomes. Finally, we partitioned the variance in demographic outcomes into contributions from UH and individual stochasticity. 4. We identify three UH groups, differing substantially in longevity, lifetime reproductive output, age at first reproduction and in the proportion of the life spent in each reproductive state. – 14% of individuals at fledging have a delayed but high probability of recruitment and extended reproductive life span. – 67% of individuals are less likely to reach adulthood, recruit late and skip breeding often but have the highest adult survival rate. – 19% of individuals recruit early and attempt to breed often. They are likely to raise their offspring successfully, but experience a relatively short life span. Unobserved heterogeneity only explains a small fraction of the variances in longevity (5.9%), age at first reproduction (3.7%) and lifetime reproduction (22%). 5. UH can affect the entire life cycle, including survival, development and reproductive rates, with consequences over the lifetime of individuals and impacts on cohort dynamics. The respective role of UH vs. individual stochasticity varies greatly among demographic outcomes. We discuss the implication of our finding for the gradient of life-history strategies observed among species and argue that individual differences should be accounted for in demographic studies of wild populations.
Climatic shifts to warmer and often drier conditions are challenging terrestrial species worldwide. These shifts are occurring more rapidly at higher elevations and latitudes, likely causing ...disproportionate effects to mammalian hibernators there. While there is some information about how these species' ranges are responding to climatic shifts, we lack an understanding of how climate components are affecting species' life history variation, which is key to individual success and population‐level resilience. We reviewed the literature to identify the direction of life history responses to climate change in mammalian hibernators along three axes: latitudinal, elevational and temporal. We found 39 studies involving 27 species that reported climate effects on our four target life history traits – phenology, body mass/condition and growth, reproduction and survival. We found warmer temperatures are advancing hibernator phenology and increasing reproductive success. By contrast, warming and drying trends are having uncertain effects on body condition, and complex effects on survival – depending on season, age class, latitude and elevation. We found no pattern of significant climate‐trait outcomes by duration or decade of study. More research on drought conditions – particularly in relation to resource availability – would help inform hibernator susceptibility to increased drying trends expected to intensify globally. Notably, our results are highly biased towards small mammal hibernators in Northern Hemisphere alpine/mountain ecosystems, with few long‐term studies conducted on Southern Hemisphere hibernators. This review highlights that phenological shifts constitute one of the most obvious consequences of climate change, yet, the timing of life history events (e.g. timing of migration, reproduction, hibernation) remains poorly understood. Further integration of insights from physiologists, evolutionary biologists and population ecologists working on wild populations will improve our collective understanding of the effects of seasonal climatic shifts on mammalian hibernator life history traits, key drivers of their population‐level persistence.
Abstract
Seasonal variation in the availability of essential resources is one of the most important drivers of natural selection on the phasing and duration of annually recurring life-cycle events. ...Shifts in seasonal timing are among the most commonly reported responses to climate change and the capacity of organisms to adjust their timing, either through phenotypic plasticity or evolution, is a critical component of resilience. Despite growing interest in documenting and forecasting the impacts of climate change on phenology, our ability to predict how individuals, populations, and species might alter their seasonal timing in response to their changing environments is constrained by limited knowledge regarding the cues animals use to adjust timing, the endogenous genetic and molecular mechanisms that transduce cues into neural and endocrine signals, and the inherent capacity of animals to alter their timing and phasing within annual cycles. Further, the fitness consequences of phenological responses are often due to biotic interactions within and across trophic levels, rather than being simple outcomes of responses to changes in the abiotic environment. Here, we review the current state of knowledge regarding the mechanisms that control seasonal timing in vertebrates, as well as the ecological and evolutionary consequences of individual, population, and species-level variation in phenological responsiveness. Understanding the causes and consequences of climate-driven phenological shifts requires combining ecological, evolutionary, and mechanistic approaches at individual, populational, and community scales. Thus, to make progress in forecasting phenological responses and demographic consequences, we need to further develop interdisciplinary networks focused on climate change science.
Anthropogenic pressure, such as urbanization and habitat loss, can wield many effects on wildlife that radiate through ecosystems. Large carnivores tend to experience these effects more severely than ...other species, diminishing their viability and altering ecosystem function by suppressing their role as an apex predator. Yet opportunistic carnivores that rely on an omnivorous diet can sometimes take advantage of anthropogenic food and improve their fitness prospects. We quantified the effect of phenotypic and ecological factors on female body mass of the American black bear (Ursus americanus) in New Jersey, USA. Habitat and reliable mast crops in New Jersey keep adult female black bear body mass and reproduction higher than many parts of the United States, and historically, female black bears in the mid‐Atlantic states tend to be larger than in other parts of their range. We used data collected from den surveys (n = 317) in northern New Jersey from 1984 to 2019 to examine the shared roles of climate, anthropogenic pressure (human food subsidies, harvest), habitat composition and configuration, natural food availability (hard mast production), and bear characteristics (age, history of human–black bear conflict) on female black bear body mass using generalized linear mixed models. Adult female body mass was heaviest with increased availability of cultivated crop and within low‐intensity developed land covers, suggesting anthropogenic food subsidies found in these 2 land cover types are contributing to female overall body mass. A history of conflict with humans explained heavier females, and a quadratic effect of age on body mass supported a senescent decline in adult female body mass later in life. Our results suggest that access to specific land cover types (i.e., crops, low‐intensity developments) that provide a diversity of food (e.g., corn, soft and hard mast) and support low human densities, explains female black bear body mass in a fragmented landscape.
We quantified the effect of phenotypic, ecological, and anthropogenic factors on American black bear female body mass using data collected from den surveys in northern New Jersey over 35 years. We examine the shared roles of bear characteristics (age, history of human‐black bear conflict), population factors (density, harvest), habitat composition and configuration, and natural food production on female body mass. Our results suggest that age, a past history of conflict behavior, and access to anthropogenic foods within land cover types with low human density support heavier females.
Invasive and overabundant species are an increasing threat to biodiversity and ecosystem functioning world‐wide. As such, large amounts of money are spent each year on attempts to control them. These ...efforts can, however, be thwarted if exploitation is compensated demographically or if populations simply become too numerous for management to elicit an effective and rapid functional response. We examined the influence of these mechanisms on cause‐specific mortality in lesser snow geese using multistate capture–reencounter methods. The abundance and destructive foraging behaviours of snow geese have created a trophic cascade that reduces (sub‐) Arctic plant, insect and avian biodiversity, bestowing them the status of ‘overabundant’. Historically, juvenile snow geese suffered from density‐related degradation of their saltmarsh brood‐rearing habitat. This allowed harvest mortality to be partially compensated by non‐harvest mortality (process correlation between mortality sources: ρ = −0·47; 90% BCI: −0·72 to −0·04). Snow goose family groups eventually responded to their own degradation of habitat by dispersing to non‐degraded areas. This relaxed the pressure of density dependence on juvenile birds, but without this mechanism for compensation, harvest began to have an additive effect on overall mortality (ρ = 0·60; 90% BCI: −0·06 to 0·81). In adults, harvest had an additive effect on overall mortality throughout the 42‐year study (ρ = 0·24; 90% BCI: −0·59 to 0·67). With the aim of controlling overabundant snow geese, the Conservation Order amendment to the International Migratory Bird Treaty was implemented in February of 1999 to allow for harvest regulations that had not been allowed since the early 1900s (e.g. a spring harvest season, high or unlimited bag limits and use of electronic calls and unplugged shotguns). Although harvest mortality momentarily increased following these actions, the increasing abundance of snow geese has since induced a state of satiation in harvest that has driven harvest rates below the long‐term average. More aggressive actions will thus be needed to halt the growth and spread of the devastating trophic cascade that snow geese have triggered. Our approach to investigating the impacts of population control efforts on cause‐specific mortality will help guide more effective management of invasive and overabundant species world‐wide.
Understanding the processes behind change in reproductive state along life‐history trajectories is a salient research program in evolutionary ecology. Two processes, state dependence and ...heterogeneity, can drive the dynamics of change among states. Both processes can operate simultaneously, begging the difficult question of how to tease them apart in practice. The Neutral Theory for Life Histories (NTLH) holds that the bulk of variations in life‐history trajectories is due to state dependence and is hence neutral: Once previous (breeding) state is taken into account, variations are mostly random. Lifetime reproductive success (LRS), the number of descendants produced over an individual's reproductive life span, has been used to infer support for NTLH in natura. Support stemmed from accurate prediction of the population‐level distribution of LRS with parameters estimated from a state dependence model. We show with Monte Carlo simulations that the current reliance of NTLH on LRS prediction in a null hypothesis framework easily leads to selecting a misspecified model, biased estimates and flawed inferences. Support for the NTLH can be spurious because of a systematic positive bias in estimated state dependence when heterogeneity is present in the data but ignored in the analysis. This bias can lead to spurious positive covariance between fitness components when there is in fact an underlying trade‐off. Furthermore, neutrality implied by NTLH needs a clarification because of a probable disjunction between its common understanding by evolutionary ecologists and its translation into statistical models of life‐history trajectories. Irrespective of what neutrality entails, testing hypotheses about the dynamics of change among states in life histories requires a multimodel framework because state dependence and heterogeneity can easily be mistaken for each other.
Two processes, state dependence and heterogeneity, can drive the dynamics of change among states in individual life‐history trajectories. A null hypothesis testing framework can easily lead to selecting misspecified models of individual trajectories. A multimodel framework is needed because state dependence and heterogeneity can easily be mistaken for each other.
The present work aimed to study whether a high sugar diet can alter immune responses and the gut microbiome in green iguanas. Thirty-six iguanas were split into four treatment groups using a 2x2 ...design. Iguanas either received a sugar supplemented diet or a control diet, and either received a lipopolysaccharide (LPS) injection or a phosphate buffer solution (PBS) injection. Iguanas were given their respective diet treatment through the entire study (∼3 months) and received a primary immune challenge one month and two months into the experiment. Blood samples and cloacal swabs were taken at various points in the experiment and used to measure changes in the immune system (bacterial killing ability, lysis and agglutination scores, LPS specific IgY concentrations), and alterations in the gut microbiome. We found that sugar diet reduces bacterial killing ability following an LPS challenge, and sugar and the immune challenge temporarily alters gut microbiome composition while reducing alpha diversity. While sugar did not directly reduce lysis and agglutination following the immune challenge, the change in these scores over a 24-hour period following an immune challenge was more drastic (it decreased) relative to the control diet group. Moreover, sugar increased constitutive agglutination outside of the immune challenges (i.e., pre-challenge levels). In this study, we provide evidence that a high sugar diet affects the immune system of green iguanas (in a disruptive manner) and alters the gut microbiome.
In Focus: Morrongiello, J. R., Sweetman, P. C., & Thresher, R. E. (2019). Fishing constrains phenotypic responses of marine fish to climate variability. Journal of Animal Ecology, 88, 1645‐1656.
...Forces of unnatural selection, such as climate change and harvest, are rarely studied in concert, yet hold the great potential to act synergistically on individual performance, susceptibility to harvest, tolerance to warming temperatures, and ultimately population persistence and resilience. In this paper, Morrongiello et al. (2019) used long‐term monitoring of a site‐attached temperate reef fish, the purple wrasse (Notolabrus fucicola), to test novel predictions about how fisheries management and climate variability could alter individual growth rates and thermal reaction norms within and across stocks. Otolith growth increments were collected from three south‐east Australian populations between 1980 and 1999, pre‐ and post‐harvest, throughout an intensive warming spell. Using hierarchical models to partition variation in growth within and between individuals and populations, Morrongiello et al. detected increased average growth rate with warming, a release from density dependence post‐harvest, and a fishing‐by‐warming interaction that decreased diversity in thermal growth reaction norms because large individuals that tend to better tolerate warm temperatures were effectively culled from the population. This study outlines the importance of determining which phenotypes are more resilient to increasing temperatures, how fisheries should manage for them, and how such collective knowledge could help preserve and even promote resilience of managed populations to increasing temperatures in ecosystems threatened by climate change.
Morrongiello et al.'s paper outlines the importance of studying reaction norms in determining which phenotypes may be more resilient to increasing temperatures, preserving such phenotypes via selective fisheries management, and using this knowledge to promote stock/population resilience to climate change in highly threatened marine ecosystems.
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