Fluctuating optimum and temporally variable selection on breeding date in birds and mammals.

Temporal variation in natural selection is predicted to strongly impact the evolution and demography of natural populations, with consequences for the rate of adaptation, evolution of plasticity, and extinction risk. Most of the theory underlying these predictions assumes a moving optimum phenotype, with predictions expressed in terms of the temporal variance and autocorrelation of this optimum. However, empirical studies seldom estimate patterns of fluctuations of an optimum phenotype, precluding further progress in connecting theory with observations. To bridge this gap, we assess the evidence for temporal variation in selection on breeding date by modeling a fitness function with a fluctuating optimum, across 39 populations of 21 wild animals, one of the largest compilations of long-term datasets with individual measurements of trait and fitness components. We find compelling evidence for fluctuations in the fitness function, causing temporal variation in the magnitude, but not the direction of selection. However, fluctuations of the optimum phenotype need not directly translate into variation in selection gradients, because their impact can be buffered by partial tracking of the optimum by the mean phenotype. Analyzing individuals that reproduce in consecutive years, we find that plastic changes track movements of the optimum phenotype across years, especially in bird species, reducing temporal variation in directional selection. This suggests that phenological plasticity has evolved to cope with fluctuations in the optimum, despite their currently modest contribution to variation in selection.

Short-term insurance versus long-term bet-hedging strategies as adaptations to variable environments.

Understanding how organisms adapt to environmental variation is a key challenge of biology. Central to this are bet-hedging strategies that maximize geometric mean fitness across generations, either by being conservative or diversifying phenotypes. Theoretical models have identified environmental variation across generations with multiplicative fitness effects as driving the evolution of bet-hedging. However, behavioral ecology has revealed adaptive responses to additive fitness effects of environmental variation within lifetimes, either through insurance or risk-sensitive strategies. Here, we explore whether the effects of adaptive insurance interact with the evolution of bet-hedging by varying the position and skew of both arithmetic and geometric mean fitness functions. We find that insurance causes the optimal phenotype to shift from the peak to down the less steeply decreasing side of the fitness function, and that conservative bet-hedging produces an additional shift on top of this, which decreases as adaptive phenotypic variation from diversifying bet-hedging increases. When diversifying bet-hedging is not an option, environmental canalization to reduce phenotypic variation is almost always favored, except where the tails of the fitness function are steeply convex and produce a novel risk-sensitive increase in phenotypic variance akin to diversifying bet-hedging. Importantly, using skewed fitness functions, we provide the first model that explicitly addresses how conservative and diversifying bet-hedging strategies might coexist.

Environmental drivers of varying selective optima in a small passerine: A multivariate, multiepisodic approach.

In changing environments, phenotypic traits are shaped by numerous agents of selection. The optimal phenotypic value maximizing the fitness of an individual thus varies through time and space with various environmental covariates. Selection may differ between different life-cycle stages and act on correlated traits inducing changes in the distribution of several traits simultaneously. Despite increasing interests in environmental sensitivity of phenotypic selection, estimating varying selective optima on various traits throughout the life cycle, while considering (a)biotic factors as potential selective agents has remained challenging. Here, we provide a statistical model to measure varying selective optima from longitudinal data. We apply our approach to analyze environmental sensitivity of phenotypic selection on egg-laying date and clutch size throughout the life cycle of a white-throated dipper population. We show the presence of a joint optimal phenotype that varies over the 35-year period, being dependent on altitude and temperature. We also find that optimal laying date is density-dependent, with high population density favoring earlier laying dates. By providing a flexible approach, widely applicable to free-ranging populations for which long-term data on individual phenotypes, fitness, and environmental factors are available, our study improves the understanding of phenotypic selection in varying environments.

Domestication and fitness in the wild: A multivariate view.

Domesticated species continually escaping and interbreeding with wild relatives impose a migration load on wild populations. As domesticated stocks become increasingly different as a result of artificial and natural selection in captivity, fitness of escapees in the wild is expected to decline, reducing the effective rate of migration into wild populations. Recent theory suggest that this may alleviate and eventually eliminate the resulting migration load. I develop a multivariate model of trait and wild fitness evolution resulting from the joint effects of artificial and natural selection in the captive environment. Initially, the evolutionary trajectory is dominated by the effects of artificial selection causing a fast initial decline in fitness of escapees in the wild. In later phases, through the counteracting effects of correlational multivariate natural selection in captivity, the mean phenotype is pushed in directions of weak stabilizing selection, allowing a sustained response in the trait subject to artificial selection. Provided that there is some alignment between the adaptive landscapes in the wild and in captivity, these phases are associated with slower rates of decline in wild fitness of the domesticated stock, suggesting that detrimental effects on wild populations are likely to remain a concern in the foreseeable future.

Estimating the variation, autocorrelation, and environmental sensitivity of phenotypic selection.

Despite considerable interest in temporal and spatial variation of phenotypic selection, very few methods allow quantifying this variation while correctly accounting for the error variance of each individual estimate. Furthermore, the available methods do not estimate the autocorrelation of phenotypic selection, which is a major determinant of eco-evolutionary dynamics in changing environments. We introduce a new method for measuring variable phenotypic selection using random regression. We rely on model selection to assess the support for stabilizing selection, and for a moving optimum that may include a trend plus (possibly autocorrelated) fluctuations. The environmental sensitivity of selection also can be estimated by including an environmental covariate. After testing our method on extensive simulations, we apply it to breeding time in a great tit population in the Netherlands. Our analysis finds support for an optimum that is well predicted by spring temperature, and occurs about 33 days before a peak in food biomass, consistent with what is known from the biology of this species. We also detect autocorrelated fluctuations in the optimum, beyond those caused by temperature and the food peak. Because our approach directly estimates parameters that appear in theoretical models, it should be particularly useful for predicting eco-evolutionary responses to environmental change.

Genetic evolution, plasticity, and bet-hedging as adaptive responses to temporally autocorrelated fluctuating selection: A quantitative genetic model.

Adaptive responses to autocorrelated environmental fluctuations through evolution in mean reaction norm elevation and slope and an independent component of the phenotypic variance are analyzed using a quantitative genetic model. Analytic approximations expressing the mutual dependencies between all three response modes are derived and solved for the joint evolutionary outcome. Both genetic evolution in reaction norm elevation and plasticity are favored by slow temporal fluctuations, with plasticity, in the absence of microenvironmental variability, being the dominant evolutionary outcome for reasonable parameter values. For fast fluctuations, tracking of the optimal phenotype through genetic evolution and plasticity is limited. If residual fluctuations in the optimal phenotype are large and stabilizing selection is strong, selection then acts to increase the phenotypic variance (bet-hedging adaptive). Otherwise, canalizing selection occurs. If the phenotypic variance increases with plasticity through the effect of microenvironmental variability, this shifts the joint evolutionary balance away from plasticity in favor of genetic evolution. If microenvironmental deviations experienced by each individual at the time of development and selection are correlated, however, more plasticity evolves. The adaptive significance of evolutionary fluctuations in plasticity and the phenotypic variance, transient evolution, and the validity of the analytic approximations are investigated using simulations.

Endoparasite infection has both short- and long-term negative effects on reproductive success of female house sparrows, as revealed by faecal parasitic egg counts.

Parasites have the potential to severely reduce host reproductive success. However, the effects of endoparasites on reproductive success have not received the same amount of attention as the effects of parasites on host survival. We investigated the relationship between an avian endoparasite (gapeworm, Syngamus trachea) and both current and future reproductive success of female house sparrows (Passer domesticus) in a population on the coast of Helgeland, northern Norway. We found that the proportion of eggs in a nest that failed to develop into fledglings increased as the faecal parasitic egg count of the mothers increased. We also found that juvenile females with high numbers of parasitic eggs in their faeces had lower lifetime reproductive success as adults. However, we did not find a relationship between maternal parasite infection and clutch size or recruitment rate of offspring. To our knowledge this is the first study to find a relationship between reproductive success of an avian host and faecal egg count of an endoparasite. The present study indicates that infection by an endoparasite may be associated with lower individual reproductive success in both the short-term and long-term in a wild population of hosts.

Temporal and spatial variation in prevalence of the parasite Syngamus trachea in a metapopulation of house sparrows (Passer domesticus).

When investigating parasite-host dynamics in wild populations, a fundamental parameter to investigate is prevalence. This quantifies the percentage of individuals infected in the population. Investigating how prevalence changes over time and space can reveal interesting aspects in the parasite-host relationship in natural populations. We investigated the dynamic between a common avian parasite (Syngamus trachea) in a host metapopulation of house sparrows (Passer domesticus) on the coast of Helgeland in northern Norway. We found that parasite prevalence varied in both time and space. In addition, the parasite prevalence was found to be different between demographic groups in the local populations. Our results reveal just how complex the dynamic between a host and its parasite may become in a fragmented landscape. Although temperature may be an important factor, the specific mechanisms causing this complexity are not fully understood, but need to be further examined to understand how parasite-host interactions may affect the ecological and evolutionary dynamics and viability of host populations.

Modelling wild-domestic interbreeding: how selection on a quantitative trait affects gene flow at a neutral locus.

Interbreeding between domesticated individuals and their wild conspecifics occurs in a range of species. The rate of gene flow into the wild population, estimated using genetic markers, is often smaller than the fraction of immigrants, as immigrants and their descendants generally have lower relative fitness. Here the difference between one-way migration rate and gene flow (effective migration rate) is explored using quantitative genetic simulations. We model a trait undergoing stabilizing selection in the recipient population, influenced by an infinite number of loci, each with small effect. Immigrants have suboptimal trait values, and differ in allele frequency at an unlinked neutral marker locus. We derive an analytical approximation for the effective migration rate, and show that in the limiting case of low migration rates, the ratio between effective and actual migration rate approximately equals the ratio between mean fitness of immigrants and in the admixed population. This ignores indirect selection on the marker locus within the admixed population due to covariance with the trait value, which may be substantial when the genetic difference between the populations is large. For higher migration rates, the gene flow/migration ratio rises with increasing migration rate, inflating the rate of gene flow.

Genetic variation and structure of house sparrow populations: is there an island effect?

Population genetic structure and intrapopulation levels of genetic variation have important implications for population dynamics and evolutionary processes. Habitat fragmentation is one of the major threats to biodiversity. It leads to smaller population sizes and reduced gene flow between populations and will thus also affect genetic structure. We use a natural system of island and mainland populations of house sparrows along the coast of Norway to characterize the different population genetic properties of fragmented populations. We genotyped 636 individuals distributed across 14 populations at 15 microsatellite loci. The level of genetic differentiation was estimated using F-statistics and specially designed Mantel tests were conducted to study the influence of population type (i.e. mainland or island) and geographic distance on the genetic population structure. Furthermore, the effects of population type, population size and latitude on the level of genetic variation within populations were examined. Our results suggest that genetic processes on islands and mainland differed in two important ways. First, the intrapopulation level of genetic variation tended to be lower and the occurrence of population bottlenecks more frequent on islands than the mainland. Second, although the general level of genetic differentiation was low to moderate, it was higher between island populations than between mainland populations. However, differentiation increased in mainland populations somewhat faster with geographical distance. These results suggest that population bottleneck events and genetic drift have been more important in shaping the genetic composition of island populations compared with populations on the mainland. Such knowledge is relevant for a better understanding of evolutionary processes and conservation of threatened populations.

Comparison of non-Gaussian quantitative genetic models for migration and stabilizing selection.

The balance between stabilizing selection and migration of maladapted individuals has formerly been modeled using a variety of quantitative genetic models of increasing complexity, including models based on a constant expressed genetic variance and models based on normality. The infinitesimal model can accommodate nonnormality and a nonconstant genetic variance as a result of linkage disequilibrium. It can be seen as a parsimonious one-parameter model that approximates the underlying genetic details well when a large number of loci are involved. Here, the performance of this model is compared to several more realistic explicit multilocus models, with either two, several or a large number of alleles per locus with unequal effect sizes. Predictions for the deviation of the population mean from the optimum are highly similar across the different models, so that the non-Gaussian infinitesimal model forms a good approximation. It does, however, generally estimate a higher genetic variance than the multilocus models, with the difference decreasing with an increasing number of loci. The difference between multilocus models depends more strongly on the effective number of loci, accounting for relative contributions of loci to the variance, than on the number of alleles per locus.

Estimating Brownian motion dispersal rate, longevity and population density from spatially explicit mark-recapture data on tropical butterflies.

1. We develop a Bayesian method for analysing mark-recapture data in continuous habitat using a model in which individuals movement paths are Brownian motions, life spans are exponentially distributed and capture events occur at given instants in time if individuals are within a certain attractive distance of the traps. 2. The joint posterior distribution of the dispersal rate, longevity, trap attraction distances and a number of latent variables representing the unobserved movement paths and time of death of all individuals is computed using Gibbs sampling. 3. An estimate of absolute local population density is obtained simply by dividing the Poisson counts of individuals captured at given points in time by the estimated total attraction area of all traps. Our approach for estimating population density in continuous habitat avoids the need to define an arbitrary effective trapping area that characterized previous mark-recapture methods in continuous habitat. 4. We applied our method to estimate spatial demography parameters in nine species of neotropical butterflies. Path analysis of interspecific variation in demographic parameters and mean wing length revealed a simple network of strong causation. Larger wing length increases dispersal rate, which in turn increases trap attraction distance. However, higher dispersal rate also decreases longevity, thus explaining the surprising observation of a negative correlation between wing length and longevity.

Does selection or genetic drift explain geographic differentiation of morphological characters in house sparrows Passer domesticus?

Understanding the relative influence of genetic drift and selection is fundamental in evolutionary biology. The theory of neutrality predicts that the genetic differentiation of a quantitative trait (QST) equals the genetic differentiation at neutral molecular markers (FST) if the quantitative trait has not been under selection. Thus, the relative magnitude of observed QST and expected QST under neutral expectations suggests the importance of selection and genetic drift for any observed phenotypic divergence. Because QST is based on additive genetic variance, estimating QST based on phenotypic measurements is problematic due to unknown environmental effects. To account for this, we used a model where the environmental component was allowed to vary when estimating QST. The model was used on data from 14 house sparrow (Passer domesticus) populations in Norway. In accordance with the significant phenotypic inter-population differences our analyses suggested that directional selection may have favoured different optimal phenotypes for some morphological traits across populations. In particular, different body mass and male ornamental phenotypes seemed to have been favoured. The conclusions are, however, dependent on assumptions regarding the proportion of the observed inter-population variation that is due to additive genetic differences, showing the importance of collecting such information in natural populations. By estimating QST, allowing the additive genetic proportion of phenotypic inter-population variation to vary, and by making use of recent statistical methods to compare observed QST with neutral expectations, we can use data that are relatively easy to collect to identify adaptive variation in natural populations.

Varying disease-mediated selection at different life-history stages of Atlantic salmon in fresh water.

Laboratory studies on associations between disease resistance and susceptibility and major histocompatibility (MH) genes in Atlantic salmon Salmo salar have shown the importance of immunogenetics in understanding the capacity of populations to fight specific diseases. However, the occurrence and virulence of pathogens may vary spatially and temporally in the wild, making it more complicated to predict the overall effect that MH genes exert on fitness of natural populations and over several life-history stages. Here we show that MH variability is a significant determinant of salmon survival in fresh water, by comparing observed and expected genotype frequencies at MH and control microsatellite loci at parr and migrant stages in the wild. We found that additive allelic effects at immunogenetic loci were more likely to determine survival than dominance deviation, and that selection on certain MH alleles varied with life stage, possibly owing to varying pathogen prevalence and/or virulence over time. Our results highlight the importance of preserving genetic diversity (particularly at MH loci) in wild populations, so that they have the best chance of adapting to new and increased disease challenges as a result of projected climate warming and increasing aquaculture.

Gene flow from domesticated species to wild relatives: migration load in a model of multivariate selection.

Domesticated species frequently spread their genes into populations of wild relatives through interbreeding. The domestication process often involves artificial selection for economically desirable traits. This can lead to an indirect response in unknown correlated traits and a reduction in fitness of domesticated individuals in the wild. Previous models for the effect of gene flow from domesticated species to wild relatives have assumed that evolution occurs in one dimension. Here, I develop a quantitative genetic model for the balance between migration and multivariate stabilizing selection. Different forms of correlational selection consistent with a given observed ratio between average fitness of domesticated and wild individuals offsets the phenotypic means at migration-selection balance away from predictions based on simpler one-dimensional models. For almost all parameter values, correlational selection leads to a reduction in the migration load. For ridge selection, this reduction arises because the distance the immigrants deviates from the local optimum in effect is reduced. For realistic parameter values, however, the effect of correlational selection on the load is small, suggesting that simpler one-dimensional models may still be adequate in terms of predicting mean population fitness and viability.

Age, size, and spatiotemporal variation in ovulation patterns of a seasonal breeder, the Norwegian moose (Alces alces).

In seasonal environments, timing of reproduction is an important fitness component. However, in ungulates, our understanding of this biological process is limited. Here we analyze how age and body mass affect spatiotemporal variation in timing of ovulation of 6,178 Norwegian moose. We introduced a parametric statistical model to obtain inferences about the seasonal timing of ovulation peak, the degree of synchrony among individuals, and the proportion of individuals that ovulate. These components showed much more spatiotemporal variation than previously reported. Young (primiparous) and old (> or =11.5 years of age) females ovulated later than prime-aged (2.5-10.5 years of age) females. In all age classes, ovulation was delayed with decreasing body mass. Ovulation rates were lower and more variable among primiparous females than among older females. Young females required higher body mass than older females did to ovulate. The body-mass-to-ovulation relationship varied with age, showed large regional variation, and differed among years within region. These results suggest that (1) environmental and population characteristics contribute to shape seasonal variation in the breeding pattern and (2) large regional variation exists in the size-dependent age at maturity in moose. Hence, the life-history trade-off between reproduction and body growth should differ regionally in moose.

The effect of collagenase and hyaluronidase on transient perfusion in human osteosarcoma xenografts grown orthotopically and in dorsal skinfold chambers.

BACKGROUND: Collagenase and hyaluronidase are enzymes which degrade the extracellular matrix and increase the uptake and improve the distribution of therapeutic macromolecules in tumours. The purpose of the present work was to investigate whether collagenase or hyaluronidase had any effects on transient perfusion and/or changes in vascular areas. MATERIALS AND METHODS: The effects were studied in human osteosarcomas in BALB/c nu/nu mice growing orthotopically around and infiltrating the femurs, and in dorsal skinfold chambers using confocal laser scanning microscopy. RESULTS: Both collagenase and hyaluronidase reduced the number of vessels that closed, but only collagenase increased the number of vessels which opened up, i.e. both enzymes improved the perfusion but collagenase to a greater extent than hyaluronidase. CONCLUSION: Destroying the structural protein network seems to be more efficient than degrading the gel of hyaluronan with respect to increase perfusion.

Dispersal of introduced house sparrows Passer domesticus: an experiment.

An important issue concerning the introduction of non-indigenous organisms into local populations is the potential of the introduced individuals to spread and interfere both demographically and genetically with the local population. Accordingly, the potential of spatial dispersal among introduced individuals compared with local individuals is a key parameter to understand the spatial and temporal dynamics of populations after an introduction event. In addition, if the variance in dispersal rate and distance is linked to individual characteristics, this may further affect the population dynamics. We conducted a large-scale experiment where we introduced 123 house sparrows from a distant population into 18 local populations without changing population density or sex ratio. Introduced individuals dispersed more frequently and over longer distances than residents. Furthermore, females had higher probability of dispersal than males. In females, there was also a positive relationship between the wing length and the probability of dispersal and dispersal distance. These results suggest that the distribution and frequency of introduced individuals may be predicted by their sex ratio as well as their phenotypic characteristics.

Natural selection acts on Atlantic salmon major histocompatibility (MH) variability in the wild.

Pathogen-driven balancing selection is thought to maintain polymorphism in major histocompatibility (MH) genes. However, there have been few empirical demonstrations of selection acting on MH loci in natural populations. To determine whether natural selection on MH genes has fitness consequences for wild Atlantic salmon in natural conditions, we compared observed genotype frequencies of Atlantic salmon (Salmo salar) surviving in a river six months after their introduction as eggs with frequencies expected from parental crosses. We found significant differences between expected and observed genotype frequencies at the MH class II alpha locus, but not at a MH class I-linked microsatellite or at seven non-MH-linked microsatellite loci. We therefore conclude that selection at the MH class II alpha locus was a result of disease-mediated natural selection, rather than any demographic event. We also show that survival was associated with additive allelic effects at the MH class II alpha locus. Our results have implications for both the conservation of wild salmon stocks and the management of disease in hatchery fish. We conclude that natural or hatchery populations have the best chance of dealing with episodic and variable disease challenges if MH genetic variation is preserved both within and among populations.

A parametric model for estimation of dispersal patterns applied to five passerine spatially structured populations.

Natal dispersal capture-recapture data from five fragmented populations of house sparrows, great tits, and blue tits were analyzed using maximum likelihood methods. A new two-parametric distribution was constructed that includes four distributions previously used as special cases in the literature. Dispersal standard deviations were estimated at 22.9 km for the house sparrows and ranged from 0.66 to 4.4 km for the tits. Female great tits and blue tits dispersed consistently further than males. Estimates of the shape parameter of the dispersal distribution ranged from 0.66 to 2.27, indicating strong to moderately leptokurtic dispersal displacements. There were significant effects of density on local immigration rates and a consistent tendency for immigration rates to depend underproportionally on local densities. Potential implications of the shape of the dispersal distribution for the spread of invading organisms were investigated and compared with previous results. It is shown that the wave speed, for a given dispersal standard deviation, depends only to some extent on leptokurtosis, provided that the intrinsic growth rate of the population is moderate or small. In estimating the dispersal standard deviation, however, incorrect assumptions about the degree of leptokurtosis can lead to a large bias in estimation and predictions.