Small-Mammal Genomics Highlights Viaducts as Potential Dispersal Conduits for Fragmented Populations.

Wildlife crossings are implemented in many countries to facilitate the dispersal of animals among habitats fragmented by roads. However, the efficacy of different types of habitat corridors remains poorly understood. We used a comprehensive sampling regime in two lowland dipterocarp forest areas in peninsular Malaysia to sample pairs of small mammal individuals in three treatment types: (1) viaduct sites, at which sampling locations were separated by a highway but connected by a vegetated viaduct; (2) non-viaduct sites, at which sampling locations were separated by a highway and not connected by a viaduct; and (3) control sites, at which there was no highway fragmenting the forest. For four small mammal species, the common tree shrew Tupaia glis, Rajah's spiny rat Maxomys rajah, Whitehead's spiny rat Maxomys whiteheadi and dark-tailed tree rat Niviventer cremoriventer, we used genome-wide markers to assess genetic diversity, gene flow and genetic structure. The differences in genetic distance across sampling settings among the four species indicate that they respond differently to the presence of highways and viaducts. Viaducts connecting forests separated by highways appear to maintain higher population connectivity than forest fragments without viaducts, at least in M. whiteheadi, but apparently not in the other species.

Critical role of insertion preference for invasion trajectory of transposons.

It is unclear how mobile DNA sequences (transposable elements, hereafter TEs) invade eukaryotic genomes and reach stable copy numbers, as transposition can decrease host fitness. This challenge is particularly stark early in the invasion of a TE family at which point hosts may lack the specialized machinery to repress the spread of these TEs. One possibility (in addition to the evolution of host regulation of TEs) is that TE families may evolve to preferentially insert into chromosomal regions that are less likely to impact host fitness. This may allow the mean TE copy number to grow while minimizing the risk for host population extinction. To test this, we constructed simulations to explore how the transposition probability and insertion preference of a TE family influence the evolution of mean TE copy number and host population size, allowing for extinction. We find that the effect of a TE family's insertion preference depends on a host's ability to regulate this TE family. Without host repression, a neutral insertion preference increases the frequency of and decreases the time to population extinction. With host repression, a preference for neutral insertions minimizes the cumulative deleterious load, increases population fitness, and, ultimately, avoids triggering an extinction vortex.

Environmental variance in male mating success modulates the positive versus negative impacts of sexual selection on genetic load.

Sexual selection on males is predicted to increase population fitness, and delay population extinction, when mating success negatively covaries with genetic load across individuals. However, such benefits of sexual selection could be counteracted by simultaneous increases in genome-wide drift resulting from reduced effective population size caused by increased variance in fitness. Resulting fixation of deleterious mutations could be greatest in small populations, and when environmental variation in mating traits partially decouples sexual selection from underlying genetic variation. The net consequences of sexual selection for genetic load and population persistence are therefore likely to be context dependent, but such variation has not been examined. We use a genetically explicit individual-based model to show that weak sexual selection can increase population persistence time compared to random mating. However, for stronger sexual selection such positive effects can be overturned by the detrimental effects of increased genome-wide drift. Furthermore, the relative strengths of mutation-purging and drift critically depend on the environmental variance in the male mating trait. Specifically, increasing environmental variance caused stronger sexual selection to elevate deleterious mutation fixation rate and mean selection coefficient, driving rapid accumulation of drift load and decreasing population persistence times. These results highlight an intricate balance between conflicting positive and negative consequences of sexual selection on genetic load, even in the absence of sexually antagonistic selection. They imply that environmental variances in key mating traits, and intrinsic genetic drift, should be properly factored into future theoretical and empirical studies of the evolution of population fitness under sexual selection.

Effect of compositional fluctuation on the survival of bet-hedging species.

Understanding the coexistence of diverse species in a changing environment is an important problem in community ecology. Bet-hedging is a strategy that helps species survive in such changing environments. However, studies of bet-hedging have often focused on the expected long-term growth rate of the species by itself, neglecting competition with other coexisting species. Here we study the extinction risk of a bet-hedging species in competition with others. We show that there are three contributions to the extinction risk. The first is the usual demographic fluctuation due to stochastic reproduction and selection processes in finite populations. The second, due to the fluctuation of population growth rate caused by environmental changes, may actually reduce the extinction risk for small populations. Besides those two, we reveal a third contribution, which is unique to bet-hedging species that diversify into multiple phenotypes: The phenotype composition of the population will fluctuate over time, resulting in increased extinction risk. We compare such compositional fluctuation to the demographic and environmental contributions, showing how they have different effects on the extinction risk depending on the population size, generation overlap, and environmental correlation.

Lizards from warm and declining populations are born with extremely short telomeres.

Aging is the price to pay for acquiring and processing energy through cellular activity and life history productivity. Climate warming can exacerbate the inherent pace of aging, as illustrated by a faster erosion of protective telomere DNA sequences. This biomarker integrates individual pace of life and parental effects through the germline, but whether intra- and intergenerational telomere dynamics underlies population trends remains an open question. Here, we investigated the covariation between life history, telomere length (TL), and extinction risk among three age classes in a cold-adapted ectotherm (Zootoca vivipara) facing warming-induced extirpations in its distribution limits. TL followed the same threshold relationships with population extinction risk at birth, maturity, and adulthood, suggesting intergenerational accumulation of accelerated aging rate in declining populations. In dwindling populations, most neonates inherited already short telomeres, suggesting they were born physiologically old and unlikely to reach recruitment. At adulthood, TL further explained females' reproductive performance, switching from an index of individual quality in stable populations to a biomarker of reproductive costs in those close to extirpation. We compiled these results to propose the aging loop hypothesis and conceptualize how climate-driven telomere shortening in ectotherms may accumulate across generations and generate tipping points before local extirpation.

A Unifying Framework for Estimating Generation Time in Age-Structured Populations: Implications for Phylogenetics and Conservation Biology.

AbstractGeneration time is a measure of the pace of life and is used to describe processes in population dynamics and evolution. We show that three commonly used mathematical definitions of generation time in age-structured populations can produce different estimates of up to several years for the same set of life history data. We present and prove a mathematical theorem that reveals a general order relation among the definitions. Furthermore, the exact population growth rate at the time of sampling influences estimates of generation time, which calls for attention. For phylogenetic estimates of divergence times between species, included demographic data should be collected when the population growth rate for each species is most common and typical. In conservation biology, demographic data should be collected during phases of population decline in declining species, contrary to common recommendations to use predisturbance data. The results can be used to improve the International Union for Conservation of Nature's recommendation in parameterizing models for evaluating threat categories of threatened species and to avoid underestimating extinction risk.

Interpreting how nonlinear diffusion affects the fate of bistable populations using a discrete modelling framework.

Understanding whether a population will survive or become extinct is a central question in population biology. One way of exploring this question is to study population dynamics using reaction-diffusion equations, where migration is usually represented as a linear diffusion term, and birth-death is represented with a nonlinear source term. While linear diffusion is most commonly employed to study migration, there are several limitations of this approach, such as the inability of linear diffusion-based models to predict a well-defined population front. One way to overcome this is to generalize the constant diffusivity, D , to a nonlinear diffusivity function D ( C ) , where C > 0 is the population density. While the choice of D ( C ) affects long-term survival or extinction of a bistable population, working solely in a continuum framework makes it difficult to understand how the choice of D ( C ) affects survival or extinction. We address this question by working with a discrete simulation model that is easy to interpret. This approach provides clear insight into how the choice of D ( C ) either encourages or suppresses population extinction relative to the classical linear diffusion model.

Scaling the extinction vortex: Body size as a predictor of population dynamics close to extinction events.

Mutual reinforcement between abiotic and biotic factors can drive small populations into a catastrophic downward spiral to extinction-a process known as the "extinction vortex." However, empirical studies investigating extinction dynamics in relation to species' traits have been lacking.We assembled a database of 35 vertebrate populations monitored to extirpation over a period of at least ten years, represented by 32 different species, including 25 birds, five mammals, and two reptiles. We supplemented these population time series with species-specific mean adult body size to investigate whether this key intrinsic trait affects the dynamics of populations declining toward extinction.We performed three analyses to quantify the effects of adult body size on three characteristics of population dynamics: time to extinction, population growth rate, and residual variability in population growth rate.Our results provide support for the existence of extinction vortex dynamics in extirpated populations. We show that populations typically decline nonlinearly to extinction, while both the rate of population decline and variability in population growth rate increase as extinction is approached. Our results also suggest that smaller-bodied species are particularly prone to the extinction vortex, with larger increases in rates of population decline and population growth rate variability when compared to larger-bodied species.Our results reaffirm and extend our understanding of extinction dynamics in real-life extirpated populations. In particular, we suggest that smaller-bodied species may be at greater risk of rapid collapse to extinction than larger-bodied species, and thus, management of smaller-bodied species should focus on maintaining higher population abundances as a priority.

Population dynamics with spatial structure and an Allee effect.

Population dynamics including a strong Allee effect describe the situation where long-term population survival or extinction depends on the initial population density. A simple mathematical model of an Allee effect is one where initial densities below the threshold lead to extinction, whereas initial densities above the threshold lead to survival. Mean-field models of population dynamics neglect spatial structure that can arise through short-range interactions, such as competition and dispersal. The influence of non-mean-field effects has not been studied in the presence of an Allee effect. To address this, we develop an individual-based model that incorporates both short-range interactions and an Allee effect. To explore the role of spatial structure we derive a mathematically tractable continuum approximation of the IBM in terms of the dynamics of spatial moments. In the limit of long-range interactions where the mean-field approximation holds, our modelling framework recovers the mean-field Allee threshold. We show that the Allee threshold is sensitive to spatial structure neglected by mean-field models. For example, there are cases where the mean-field model predicts extinction but the population actually survives. Through simulations we show that our new spatial moment dynamics model accurately captures the modified Allee threshold in the presence of spatial structure.

Sperm storage reduces the strength of the mate-finding Allee effect.

Mate searching is a key component of sexual reproduction that can have important implications for population viability, especially for the mate-finding Allee effect. Interannual sperm storage by females may be an adaptation that potentially attenuates mate limitation, but the demographic consequences of this functional trait have not been studied. Our goal is to assess the effect of female sperm storage durability on the strength of the mate-finding Allee effect and the viability of populations subject to low population density and habitat alteration. We used an individual-based simulation model that incorporates realistic representations of the demographic and spatial processes of our model species, the spur-thighed tortoise (Testudo graeca). This allowed for a detailed assessment of reproductive rates, population growth rates, and extinction probabilities. We also studied the relationship between the number of reproductive males and the reproductive rates for scenarios combining different levels of sperm storage durability, initial population density, and landscape alteration. Our results showed that simulated populations parameterized with the field-observed demographic rates collapsed for short sperm storage durability, but were viable for a durability of one year or longer. In contrast, the simulated populations with a low initial density were only viable in human-altered landscapes for sperm storage durability of 4 years. We find that sperm storage is an effective mechanism that can reduce the strength of the mate-finding Allee effect and contribute to the persistence of low-density populations. Our study highlights the key role of sperm storage in the dynamics of species with limited movement ability to facilitate reproduction in patchy landscapes or during population expansion. This study represents the first quantification of the effect of sperm storage durability on population dynamics in different landscapes and population scenarios.

How frequency-dependent selection affects population fitness, maladaptation and evolutionary rescue.

Frequency-dependent (FD) selection is a central process maintaining genetic variation and mediating evolution of population fitness. FD selection has attracted interest from researchers in a wide range of biological subdisciplines, including evolutionary genetics, behavioural ecology and, more recently, community ecology. However, the implications of frequency dependence for applied biological problems, particularly maladaptation, biological conservation and evolutionary rescue remain underexplored. The neglect of FD selection in conservation is particularly unfortunate. Classical theory, dating back to the 1940s, demonstrated that frequency dependence can either increase or decrease population fitness. These evolutionary consequences of FD selection are relevant to modern concerns about population persistence and the capacity of evolution to alleviate extinction risks. But exactly when should we expect FD selection to increase versus decrease absolute fitness and population growth? And how much of an impact is FD selection expected to have on population persistence versus extinction in changing environments? The answers to these questions have implications for evolutionary rescue under climate change and may inform strategies for managing threatened populations. Here, we revisit the core theory of FD selection, reviewing classical single-locus models of population genetic change and outlining short- and long-run consequences of FD selection for the evolution of population fitness. We then develop a quantitative genetic model of evolutionary rescue in a deteriorating environment, with population persistence hinging upon the evolution of a quantitative trait subject to both frequency-dependent and frequency-independent natural selection. We discuss the empirical literature pertinent to this theory, which supports key assumptions of our model. We show that FD selection can promote population persistence when it aligns with the direction of frequency-independent selection imposed by abiotic environmental conditions. However, under most scenarios of environmental change, FD selection limits a population's evolutionary responsiveness to changing conditions and narrows the rate of environmental change that is evolutionarily tolerable.

Phenotypic lag and population extinction in the moving-optimum model: insights from a small-jumps limit.

Continuous environmental change-such as slowly rising temperatures-may create permanent maladaptation of natural populations: Even if a population adapts evolutionarily, its mean phenotype will usually lag behind the phenotype favored in the current environment, and if the resulting phenotypic lag becomes too large, the population risks extinction. We analyze this scenario using a moving-optimum model, in which one or more quantitative traits are under stabilizing selection towards an optimal value that increases at a constant rate. We have recently shown that, in the limit of infinitely small mutations and high mutation rate, the evolution of the phenotypic lag converges to an Ornstein-Uhlenbeck process around a long-term equilibrium value. Both the mean and the variance of this equilibrium lag have simple analytical formulas. Here, we study the properties of this limit and compare it to simulations of an evolving population with finite mutational effects. We find that the "small-jumps limit" provides a reasonable approximation, provided the mean lag is so large that the optimum cannot be reached by a single mutation. This is the case for fast environmental change and/or weak selection. Our analysis also provides insights into population extinction: Even if the mean lag is small enough to allow a positive growth rate, stochastic fluctuations of the lag will eventually cause extinction. We show that the time until this event follows an exponential distribution, whose mean depends strongly on a composite parameter that relates the speed of environmental change to the adaptive potential of the population.

Early warning signals detect critical impacts of experimental warming.

Earth's surface temperatures are projected to increase by ~1-4°C over the next century, threatening the future of global biodiversity and ecosystem stability. While this has fueled major progress in the field of physiological trait responses to warming, it is currently unclear whether routine population monitoring data can be used to predict temperature-induced population collapse. Here, we integrate trait performance theory with that of critical tipping points to test whether early warning signals can be reliably used to anticipate thermally induced extinction events. We find that a model parameterized by experimental growth rates exhibits critical slowing down in the vicinity of an experimentally tested critical threshold, suggesting that dynamical early warning signals may be useful in detecting the potentially precipitous onset of population collapse due to global climate change.

Mathematical Modeling of Extinction of Inhomogeneous Populations.

Mathematical models of population extinction have a variety of applications in such areas as ecology, paleontology and conservation biology. Here we propose and investigate two types of sub-exponential models of population extinction. Unlike the more traditional exponential models, the life duration of sub-exponential models is finite. In the first model, the population is assumed to be composed of clones that are independent from each other. In the second model, we assume that the size of the population as a whole decreases according to the sub-exponential equation. We then investigate the "unobserved heterogeneity," i.e., the underlying inhomogeneous population model, and calculate the distribution of frequencies of clones for both models. We show that the dynamics of frequencies in the first model is governed by the principle of minimum of Tsallis information loss. In the second model, the notion of "internal population time" is proposed; with respect to the internal time, the dynamics of frequencies is governed by the principle of minimum of Shannon information loss. The results of this analysis show that the principle of minimum of information loss is the underlying law for the evolution of a broad class of models of population extinction. Finally, we propose a possible application of this modeling framework to mechanisms underlying time perception.

Hard harvesting of a stochastically changing population.

We consider a population whose size changes stochastically under a branching process, with the added modification that each generation a fixed number of individuals are removed, irrespective of the size of the population. We call removal that is independent of population size 'hard harvesting'. A key feature of hard harvesting occurs if the size of the population is smaller than the fixed number that are harvested. In such a case, the dynamics cannot continue and must terminate. We find that even for populations with a tendency to grow, there is a finite probability of termination. We determine the probability of termination, and given that termination occurs, we characterise the statistical properties of the random time to termination. We determine the impact of hard harvesting on the size of the population, in populations where termination has not occurred.

Whitemouth croaker, Micropogonias furnieri, trapped in a freshwater coastal lagoon: a natural comparison of freshwater and marine influences on otolith chemistry

Strontium and barium incorporation into otoliths was compared between whitemouth croaker, Micropogonias furnieri, collected from an entrapped freshwater population (Mirim Lagoon) and a normal marine/estuarine population in southern Brazil. Chemical analysis was performed using LA-ICPMS with the objective of validating the effects of marine and freshwater environments on Sr and Ba incorporation as a basis for further investigation of marine and freshwater connectivity of M. furnieri. The freshwater population was dominated by older fish with mean ±SD age of 34±1 y, whereas the coastal samples were dominated by younger fish of 14±7 y. Comparison of strontium and barium incorporation among otolith life-history profiles indicated significantly higher barium and lower strontium for the freshwater population compared to the marine population. Furthermore, comparison of otolith material deposited in the freshwater, estuarine and marine life-history phases demonstrated clear differences among these environments. Mean concentrations of strontium and barium in otoliths of M. furnieri were respectively 710 and 112 µg g-1 for freshwater, 2069 and 16.7 µg g-1 for estuarine, and 2990 and 2.7 µg g-1 for marine life-history phases. Barium concentrations in otoliths from the freshwater population of M. furnieri appeared high relative to other freshwater species. Strontium levels across life-history profiles of marine fish increased with age from 2000 to 2900 µg g-1, possibly indicating more time spent in marine than estuarine waters with age. In contrast, for the freshwater population, strontium levels decreased during the first year of life approximately to 700 µg g-1, and remained low and stable thereafter, consistent with the early life-history occurring in an estuarine environment prior to entrapment in Mirim Lagoon. The results confirm the strong and opposite effects of marine and freshwater environments on incorporation of barium and strontium into...

Estrôncio e bário foram determinados em otólitos de corvina Micropogonias furnieri coletados em habitats de água doce (lagoa Mirim) e costeiros no Sul Brasil. As análises foram realizadas utilizando-se LA-ICPMS, com o objetivo de estabelecer assinaturas químicas específicas para os diferentes habitats e avaliar a aplicabilidade da química de otólitos para o estudo de mudanças de habitat na espécie em questão para futuros estudos sobre conectividade de populações. Os animais coletados na lagoa Mirim apresentaram idade média de 34±1 anos, não sendo observados adultos jovens ou juvenis. Foi verificada uma variação significativa nas concentrações de Sr e Ba em otólitos para áreas marinhas e de água doce. Para ambientes marinhos, a idade média foi de 14±7 anos. Os valores médios de Sr e Ba foram estimados, respectivamente, em 710 e 112 µg g-1 para água doce, 2069 e 16,7 µg g-1 para água estuarina e 2990 e 2,7 µg g-1 para águas costeiras. Nos otólitos provenientes dos indivíduos de água doce, o Ba apresentou concentrações mais altas quando comparado a valores observados para outras espécies. Observou-se que a incorporação de Ba nos otólitos ao longo da vida sofre certa influência ontogenética, com valores mais altos medidos no início da vida. As concentrações de Sr em otólitos de animais costeiros aumentaram em média de 2000 a 2900 µg g-1 ao longo da vida, indicando a mudança de habitats estuarinos para marinhos. Para água doce, a concentração de Sr decresce antes do primeiro ano até valores em torno de 700 µg g-1 mantendo essa concentração por toda a vida, indicando um ambiente de água doce estável. Estes resultados confirmam o forte efeito inverso que ambientes marinhos e de água doce promovem na incorporação de Sr e Ba em otólitos e permitem sugerir que a corvina encontrada na lagoa Mirim é representada por um grupo isolado de animais com baixa probabilidade de reprodução que, portanto, será possivelmente extinto nos próximos anos.