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Biology subjects

Reid, J. M.

Publications and source records attributed to Reid, J. M..

10 recordsLinked to original sources

Conceptualising and quantifying phenological plasticity through latent responses to seasonal environmental progression

Quantifying how individuals adjust the seasonal timings of life-history events (i.e. their phenology) in response to seasonal environmental conditions is fundamental to predicting impacts of changing seasonality. However, the current standard approach of inferring phenological responses by directly analysing observed event dates relies on foundational assumptions that could be invalidated by changing seasonality, and excludes individuals that do not express focal events, potentially generating misleading inferences. To overcome these limitations, we devised a Phenological Threshold Model (PTM) that conceptualizes phenological events as switches between discrete life-history states and primarily estimates variation in underlying latent dynamic responses to seasonal progression, from which event dates secondarily arise. We demonstrate that the PTM can accurately retrieve simulated parameter values, including given incomplete seasonal field observations. Application to multi-year data on annual breeding in black-legged kittiwakes (Rissa tridactyla) demonstrated substantial among-individual variation in latent responses to seasonally varying environmental drivers, and associated daily probabilities that individuals will initiate breeding, revealing how annual distributions of breeding dates and proportions of non-breeders jointly arise. We thereby formalise a new conceptual and statistical framework for quantifying the potential for, and constraints on, rapid plastic and micro-evolutionary changes in phenology in changing seasonal climatic and environmental regimes.

ecology↗

Extreme climatic events shape adaptive potential by altering genetic variance for adult survival in a wild population

Extreme climatic events (ECEs) could potentially induce episodes of rapid adaptive evolution, altering the evolutionary trajectories and viability of wild populations experiencing increasingly stochastic environments. Adaptive potential stems substantially from additive genetic variance (V) in survival. However, the degree to which ECEs impact this variance, and the resulting evolutionary implications, have not been fully conceptualised or quantified in nature. These aims are highly challenging because underlying genetic and environmental variances have fundamentally non-linear effects on the dichotomous phenotypic outcome of survival versus death, while substantial data are required for estimation. We present a conceptual and analytical framework that formalises biological hypotheses for how V depends on environmental severity, how such dependences are reshaped by non-linear genotype-environment-phenotype relationships and demographic structure, and the implications for evolutionary responses. We then use 25 years of survival and pedigree data from European shags (Gulosus aristotelis) to decompose variance in adult survival across diverse environmental conditions including ECEs. Using a capture-recapture animal model, we demonstrate non-negligible V underlying adult survival across all years combined, implying notable adaptive potential. Yet, partitioning by environmental severity revealed substantial V in good years with high survival but negligible V in bad years with ECE-induced low survival, implying a genotype-by-environment interaction that constrains adaptive potential under severe conditions. However, scale transformations showed how the non-linear genotype-environment-phenotype relationship can distort or even reverse such patterns, by reducing the extent to which V is phenotypically expressed in good conditions with high mean survival and amplifying it in more severe conditions with lower mean survival. Evolutionary responses to severe conditions could consequently be non-negligible even given small underlying V. We thereby demonstrate how ECEs can reshape adaptive potential, highlighting the need to integrate impacts of environmental severity on genetic variation in fitness components into predictions of population resilience under climate change.

evolutionary biology↗

Eco-evolutionary dynamics of partially migratory metapopulations in spatially and seasonally varying environments

Predicting population responses to environmental changes requires understanding interactions among environmentally induced phenotypic variation, selection, demography and genetic variation, and thereby predicting eco-evolutionary dynamics emerging across diverse temporal and spatial scales. Partially migratory metapopulations (PMMPs), featuring seasonal coexistence of resident and migrant individuals across multiple spatially distinct subpopulations, have clear potential for complex spatio-seasonal eco-evolutionary dynamics through impacts of selection on migration on spatial population dynamics, and feedbacks resulting from ongoing micro-evolution. However, the key genetic and environmental conditions that maintain migratory polymorphisms, and eco-evolutionary dynamics of PMMPs under stochastic environmental variation and strong seasonal perturbations, have not yet been resolved. Accordingly, we present a general individual-based model that tracks eco-evolutionary dynamics in PMMPs inhabiting spatially structured, seasonally varying landscapes, with migration formulated as a quantitative genetic threshold trait. Our simulations show that such genetic and landscape structures, which commonly occur in nature, can readily produce a variety of stable partially migratory systems given diverse regimes of spatio-seasonal environmental variation. Typically, partial migration is maintained whenever sites differ in non-breeding season suitability resulting from variation in density-dependence, causing ideal free non-breeding distributions where residents and migrants occur with frequencies that generate similar survival probabilities. Yet, stable partial migration can also arise without any fixed differences in non-breeding season density-dependence among sites, and even without density-dependence at all, through risk-spreading given sufficiently large stochastic environmental fluctuations among sites and years. Finally, we show that local non-breeding season mortality events, as could result from extreme climatic events, can generate eco-evolutionary dynamics that ripple out to affect breeding and non-breeding season space use of subpopulations throughout the PMMP, on both short and longer timeframes. Such effects result from spatially divergent selection on both the occurrence and destinations of migration. Our model thus shows how facultative seasonal migration can act as a key mediator of eco-evolutionary dynamics in spatially and seasonally structured environments, providing key steps towards predicting responses of natural partially migratory populations to ongoing changes in spatio-seasonal patterns of environmental variation.

evolutionary biology↗

Components of micro-evolutionary and phenotypic change in seasonal migration versus residence in a wild population

Dissecting joint micro-evolutionary and plastic responses to environmental perturbations fundamentally requires quantifying interacting components of genetic and environmental variation underlying expression of key traits. This ambition is particularly challenging for phenotypically discrete traits where multiscale decompositions are required to handle non-linear transformations of underlying genetic and environmental variation into phenotypic variation, especially when effects have to be estimated from incomplete field observations. We devised a novel joint multistate capture-recapture and quantitative genetic animal model, and fitted this model to full-annual-cycle resighting data from partially migratory European shags (Gulosus aristotelis) to estimate key components of genetic, environmental and phenotypic variance in the ecologically critical discrete trait of seasonal migration versus residence. We demonstrate non-trivial additive genetic variance in latent liability for migration, resulting in estimated micro-evolutionary responses following two episodes of strong survival selection. Yet, underlying additive genetic effects interacted with substantial permanent individual and temporary environmental effects to generate complex non-additive effects, causing large intrinsic gene-by-environment interaction variance in phenotypic expression. Our findings reveal how temporal dynamics of seasonal migration result from combinations of instantaneous micro-evolution and within-individual phenotypic inertia, and highlight how plastic phenotypic variation could expose cryptic genetic variation underlying discrete traits to complex forms of selection.

evolutionary biology↗

Strong spatial population structure shapes the temporal coevolutionary dynamics of costly female preference and male display

Female mating preferences for exaggerated male display traits are commonplace. Yet, comprehensive understanding of the evolution and persistence of costly female preference through indirect (Fisherian) selection in finite populations requires some explanation for the persistence of additive genetic variance (Va) underlying sexual traits, given that directional preference is expected to deplete Va in display and hence halt preference evolution. However, the degree to which Va, and hence preference-display coevolution, may be prolonged by spatially variable sexual selection arising solely from limited gene flow and genetic drift within spatially structured populations has not been examined. Our genetically and spatially explicit model shows that spatial population structure arising in an ecologically homogeneous environment can facilitate evolution and long-term persistence of costly preference given small subpopulations and low dispersal probabilities. Here, genetic drift initially creates spatial variation in female preference, leading to persistence of Va in display through "migration-bias" of genotypes maladapted to emerging local sexual selection, thus fuelling coevolution of costly preference and display. However, costs of sexual selection increased the probability of subpopulation extinction, limiting persistence of high preference-display genotypes. Understanding long-term dynamics of sexual selection systems therefore requires joint consideration of coevolution of sexual traits and metapopulation dynamics.

evolutionary biology↗

Partial inhibition of mitochondrial complex I attenuates neurodegeneration and restores energy homeostasis and synaptic function in a symptomatic Alzheimers mouse model

We demonstrate that mitochondrial respiratory chain complex I is an important small molecule druggable target in Alzheimers Disease (AD). Partial inhibition of complex I triggers the AMP-activated protein kinase-dependent signaling network leading to neuroprotection in symptomatic APP/PS1 mice, a translational model of AD. Treatment of APP/PS1 mice with complex I inhibitor after the onset of AD-like neuropathology improved energy homeostasis, synaptic activity, long-term potentiation, dendritic spine maturation, cognitive function and proteostasis, and reduced oxidative stress and inflammation in brain and periphery, ultimately blocking the ongoing neurodegeneration. Therapeutic efficacy in vivo was monitored using translational biomarkers FDG-PET, 31P NMR, and metabolomics. Cross-validation of the mouse and the human AMP-AD transcriptomic data demonstrated that pathways improved by the treatment in APP/PS1 mice, including the immune system response and neurotransmission, represent mechanisms essential for therapeutic efficacy in AD patients.

neuroscience↗

Sex-specific additive genetic variances and correlations for fitness in a song sparrow (Melospiza melodia) population subject to natural immigration and inbreeding

Quantifying sex-specific additive genetic variance (VA) in fitness, and the cross-sex genetic correlation (rA), is pre-requisite to predicting evolutionary dynamics and the magnitude of sexual conflict. Quantifying VA and rA in underlying fitness components, and multiple genetic consequences of immigration and resulting gene flow, is required to identify mechanisms that maintain VA in fitness. However, these key parameters have rarely been estimated in wild populations experiencing natural environmental variation and immigration. We used comprehensive pedigree and life-history data from song sparrows (Melospiza melodia) to estimate VA and rA in sex-specific fitness and underlying fitness components, and to estimate additive genetic effects of immigrants as well as inbreeding depression. We found substantial VA in female and male fitness, with a moderate positive cross-sex rA. There was also substantial VA in adult reproductive success in males but not females, and moderate VA in juvenile survival but not adult survival. Immigrants introduced alleles for which additive genetic effects on local fitness were negative, potentially reducing population mean fitness through migration load, yet alleviating expression of inbreeding depression. Substantial VA for fitness can consequently be maintained in the wild, and be concordant between the sexes despite marked sex-specific VA in reproductive success.

evolutionary biology↗

Individual repeatability and heritability of divorce in a wild population

Understanding micro-evolutionary responses of mating systems to contemporary selection requires estimating sex-specific additive genetic variances and cross-sex genetic covariances in key reproductive strategy traits. One key trait comprises the occurrence of divorce versus mate-fidelity across sequential reproductive attempts. If divorce represents an evolving behavioural strategy it must have non-zero individual repeatability and heritability, but quantitative estimates from wild populations are scarce. We used 39 years of individual breeding records and pedigree data from free-living song sparrows (Melospiza melodia) to quantify sex-specific permanent individual and additive genetic variances, and hence estimate repeatability and heritability, in liability for divorce. We estimated moderate repeatability in females, but little repeatability in males. Estimates of additive genetic variance were small in both sexes, and the cross-sex genetic covariance was close to zero. However, the total heritability was likely non-zero but small, indicating low potential for micro-evolutionary response to selection. Rapid micro-evolution of divorce rate therefore appears unlikely, even if there were substantial fitness benefits of divorce and resulting selection.

evolutionary biology↗

The consequences of polyandry for sibship structures, distributions of relationships and relatedness, and potential for inbreeding in a wild population

The evolutionary benefits of simultaneous polyandry (female multiple mating within a single reproductive event) remain elusive. One potential benefit could arise if polyandry alters sibship structures and consequent relationships and relatedness among females descendants, and thereby intrinsically reduces future inbreeding risk (the indirect inbreeding avoidance hypothesis). However such effects have not been quantified in naturally complex reproductive systems that also encompass iteroparity, overlapping generations, sequential polyandry, and polygyny. We used long-term social and genetic pedigree data from song sparrows (Melospiza melodia) to quantify cross-generational consequences of simultaneous polyandry for offspring sibship structures and distributions of relationships and relatedness among possible mates. Simultaneous polyandry decreased full-sibships and increased half-sibships on average, but such effects varied among females and were smaller than would occur in the absence of sequential polyandry or polygyny. Further, while simultaneous polyandry decreased the overall frequencies of possible matings among adult full-sibs, it increased the frequencies of possible matings among adult half-sibs and more distant relatives. These results imply that the intrinsic consequences of simultaneous polyandry for inbreeding risk could cause weak indirect selection on polyandry, but the magnitude and direction of such effects will depend on complex interactions with other mating system components and the form of inbreeding depression.

evolutionary biology↗

Evolution Of Pre-Copulatory And Post-Copulatory Strategies Of Inbreeding Avoidance And Associated Polyandry

Inbreeding depression is widely hypothesised to drive adaptive evolution of pre-copulatory and post-copulatory mechanisms of inbreeding avoidance, which in turn are hypothesised to affect evolution of polyandry (i.e., female multiple mating). However, surprisingly little theory or modelling critically examines selection for pre-copulatory or post-copulatory inbreeding avoidance, or both strategies, given evolutionary constraints and direct costs, or examines how evolution of inbreeding avoidance strategies might feed back to affect evolution of polyandry. Selection for post-copulatory inbreeding avoidance, but not for pre-copulatory inbreeding avoidance, requires polyandry, while interactions between pre-copulatory and post-copulatory inbreeding avoidance might cause functional redundancy (i.e., degeneracy) potentially generating complex evolutionary dynamics among inbreeding strategies and polyandry. We used individual-based modelling to quantify evolution of interacting pre-copulatory and post-copulatory inbreeding avoidance and associated polyandry given strong inbreeding depression and different evolutionary constraints and direct costs. We found that evolution of post-copulatory inbreeding avoidance increased selection for initially rare polyandry, and that evolution of a costly inbreeding avoidance strategy became negligible over time given a lower cost alternative strategy. Further, fixed pre-copulatory inbreeding avoidance often completely precluded evolution of polyandry and hence post-copulatory inbreeding avoidance, but fixed post-copulatory inbreeding avoidance did not preclude evolution of pre-copulatory inbreeding avoidance. Evolution of inbreeding avoidance phenotypes and associated polyandry are therefore affected by evolutionary feedbacks and degeneracy. All else being equal, evolution of pre-copulatory inbreeding avoidance and resulting low polyandry is more likely when post-copulatory inbreeding avoidance is precluded or costly, and evolution of post-copulatory inbreeding avoidance greatly facilitates evolution of costly polyandry.

evolutionary biology↗