Interactive effects of environmental stress and inbreeding on reproductive traits in a wild bird population

1. Conservation biologists are concerned about the interactive effects of environmental stress and inbreeding because such interactions could affect the dynamics and extinction risk of small and isolated populations, but few studies have tested for these interactions in nature. 2. We used data from the long-term population study of song sparrows Melospiza melodia on Mandarte Island to examine the joint effects of inbreeding and environmental stress on four fitness traits that are known to be affected by the inbreeding level of adult birds: hatching success, laying date, male mating success and fledgling survival. 3. We found that inbreeding depression interacted with environmental stress to reduce hatching success in the nests of inbred females during periods of rain. 4. For laying date, we found equivocal support for an interaction between parental inbreeding and environmental stress. In this case, however, inbred females experienced less inbreeding depression in more stressful, cooler years. 5. For two other traits, we found no evidence that the strength of inbreeding depression varied with environmental stress. First, mated males fathered fewer nests per season if inbred or if the ratio of males to females in the population was high, but inbreeding depression did not depend on sex ratio. Second, fledglings survived poorly during rainy periods and if their father was inbred, but the effects of paternal inbreeding and rain did not interact. 6. Thus, even for a single species, interactions between the inbreeding level and environmental stress may not occur in all traits affected by inbreeding depression, and interactions that do occur will not always act synergistically to further decrease fitness.     

High genetic variation in leopards indicates large and long-term stable effective population size

In this paper we employ recently developed statistical and molecular tools to analyse the population history of the Tanzanian leopard (Panthera pardus), a large solitary felid. Because of their solitary lifestyle little is known of their past or present population dynamics. Eighty-one individuals were scored at 18 microsatellite loci. Overall, levels of heterozygosity were high (0.77 +/- 0.03), with a small heterozygote deficiency (0.06 +/- 0.03). Effective population size (Ne) was calculated to be 38 000-48 000. A Ne:N ratio of 0.42 (average from four cat studies) gives a present population size of about 100 000 leopards in Tanzania. Four different bottleneck tests indicated that this population has been large and stable for a minimum of several thousand years. FST values were low and no significant genetic structuring of the population could be detected. This concurs well with the large migration values (Nm) obtained (>3.3 individuals/generation). Our analysis reveals that ecological factors (e.g. disease), which are known to have had major impact on other carnivore populations, are unlikely to have impacted strongly on the population dynamics of Tanzanian leopards. The explanation may be found in their solitary life-style, their often nonconfrontational behaviour toward interspecific competitors, or that any bottlenecks have been of limited size, localized, or too short to have affected genetic variation to any measurable degree. Since the genetic structuring is weak, gene flow is not restricted to within protected areas. Local loss of genetic variation is therefore not of immediate concern.     

Bottlenecks in large populations: the effect of immigration on population viability

We model a large population that is subject to successive short bottlenecks, in order to investigate the impact of different extents of immigration on the change in genetic load and on viability. A first simple genetic model uncovers the opposite effects of immigration on fitness according to the type of deleterious mutations considered: immigration increases fitness if the genetic load is comprised of mildly deleterious mutations, whereas it decreases fitness if it is comprised of lethals. When considering both types of mutations and adding explicit stochastic demographic considerations, in which bottlenecks are engendered by random catastrophes, the global impact of immigration on viability is dependent upon a balance between its opposite effects on the two components of the genetic load and on demographic stochasticity. In this context, immigration tends to increase the probability of extinction if occurring preferentially when population density is high, while it decreases extinction if occurring preferentially towards low-density populations.     

Optimizing the genetic composition of a translocation population: Incorporating constraints and conflicting objectives

Translocations of threatened species can reduce the risk of extinction from a catastrophic event. For plants, translocation consists of moving individuals, seeds, or cuttings from a native (source) population to a new site. Ideally a translocation population would be genetically diverse and consist of fit founding individuals. In practice, there are challenges to designing such a population, including constraints on the availability of material, and tradeoffs between different goals. Here, we present an approach for designing a translocation population that identifies sets of founders that are optimized according to multiple criteria (e.g., genetic diversity), while also conforming to constraints on the representation of different founders (e.g., propagation success). It uses flexible inputs, including SNP genotypes, matrices of similarity between individuals, and vectors of phenotype data. We apply the approach to a critically endangered plant, Hibbertia puberula subsp. glabrescens (Dilleniaceae), which was genotyped at thousands of SNP loci. The goals of minimizing genetic similarity among the founding individuals and maximizing genetic diversity were largely complementary: populations optimized for one of these criteria were near‐optimal for the other. We also performed analyses in which we minimized genetic similarity among founding individuals while imposing selection (against hypothetical deleterious alleles, and against undesirable phenotypes, respectively), and here characterized sharp tradeoffs. This was useful in allowing the benefits of selection to be weighed against costs in terms of genetic similarity. In summary, we present an approach for designing a translocation population that allows flexible inputs, the imposition of realistic constraints, and examination of conflicting goals.     

Differential effects of abandonment on the demography of the grassland perennial Succisa pratensis

Abandonment of traditional land-use practices can have strong effects on the abundance of species occurring in agricultural landscapes. However, the precise mechanisms by which individual performance and population dynamics are affected are still poorly understood. To assess how abandonment affects population dynamics of Succisa pratensis we used data from a 4-year field study in both abandoned and traditionally grazed areas in moist and mesic habitats to parameterize integral projection models. Abandoned populations had a lower long-term stochastic population growth rate (λ _S = 0.90) than traditionally managed populations (λ _S = 1.08), while λ _S did not differ between habitat types. The effect of abandonment differed significantly between years and had opposed effects on different vital rates. Individuals in abandoned populations experienced higher mortality rates and lower seedling establishment, but had higher growth rates and produced more flower heads per plant. Population viability analyses, based on a population survey of the whole study area in combination with our demographic models, showed that 32 % of the populations face a high risk of extinction (>80 %) within 20 years. These results suggest that immediate changes in management are needed to avoid extinctions and further declines in population sizes. Stochastic elasticity analyses and stochastic life table response experiments indicated that management strategies would be most effective if they increase survival of small plants as well as seedling establishment, while maintaining a high seed production. This may be achieved by varying the grazing intensity between years or excluding grazers when plants are flowering.     

Relationship between population size, allozyme variation, and plant performance in the narrow endemic Cochlearia bavarica

We studied population viability in relation topopulation size and allelic variation in thenarrowly-endemic, monocarpic perennial plantCochlearia bavarica in Bavaria. In 1996,we analysed allelic variation by allozymeelectrophoresis in 24 populations ranging from8–2000 flowering individuals. Fitness-relatedcharacters were investigated in 22 of the 24populations in the field in 1996 (reproductiveand vegetative traits) and 1998 (reproductivetraits only). Differences in allozyme patternwere large between a south-eastern and awestern population group. Genetic diversity,assessed by the Shannon-Wiener diversity index,was low within but high among populations.Small populations had fewer alleles per locus,fewer polymorphic loci, lower observedheterozygosity, and lower genetic diversitythan large populations. Environmentalvariables were not significantly correlatedwith population size or fitness with theexception of light availability, indicatingthat habitat quality was similar for large andsmall populations. Population size showedpositive correlations with number of flowers,fruit set per plant, number of seeds per fruit,and total seed output per plant. Fruit set andnumber of seeds per fruit were positivelycorrelated with the observed heterozygosity andthe proportion of polymorphic loci. We usedpath analyses to study the possible causalrelationships among population size, allelicvariation, and reproductive characters. Thesemodels showed that allelic variation had nodirect influence on reproductive characters,whereas population size did. We conclude thatat present population size reduces viabilityand also reduces allelic variation; but thereduced allelic variation may in the longerterm have negative feed-backs on bothpopulation size and viability.     

The genealogy and genetic viability of reintroduced Yellowstone grey wolves

The recovery of the grey wolf in Yellowstone National Park is an outstanding example of a successful reintroduction. A general question concerning reintroduction is the degree to which genetic variation has been preserved and the specific behavioural mechanisms that enhance the preservation of genetic diversity and reduce inbreeding. We have analysed 200 Yellowstone wolves, including all 31 founders, for variation in 26 microsatellite loci over the 10-year reintroduction period (1995-2004). The population maintained high levels of variation (1995 H(0) = 0.69; 2004 H(0) = 0.73) with low levels of inbreeding (1995 F(IS) = -0.063; 2004 F(IS) = -0.051) and throughout, the population expanded rapidly (N(1995) = 21; N(2004) = 169). Pedigree-based effective population size ratios did not vary appreciably over the duration of population expansion (1995 N(e)/N(g) = 0.29; 2000 N(e)/N(g) = 0.26; 2004 N(e)/N(g) = 0.33). We estimated kinship and found only two of 30 natural breeding pairs showed evidence of being related (average r = -0.026, SE = 0.03). We reconstructed the genealogy of 200 wolves based on genetic and field data and discovered that they avoid inbreeding through a wide variety of behavioural mechanisms including absolute avoidance of breeding with related pack members, male-biased dispersal to packs where they breed with nonrelatives, and female-biased subordinate breeding. We documented a greater diversity of such population assembly patterns in Yellowstone than previously observed in any other natural wolf population. Inbreeding avoidance is nearly absolute despite the high probability of within-pack inbreeding opportunities and extensive interpack kinship ties between adjacent packs. Simulations showed that the Yellowstone population has levels of genetic variation similar to that of a population managed for high variation and low inbreeding, and greater than that expected for random breeding within packs or across the entire breeding pool. Although short-term losses in variation seem minimal, future projections of the population at carrying capacity suggest significant inbreeding depression will occur without connectivity and migratory exchange with other populations.     

Source population characteristics affect heterosis following genetic rescue of fragmented plant populations

Understanding the relative importance of heterosis and outbreeding depression over multiple generations is a key question in evolutionary biology and is essential for identifying appropriate genetic sources for population and ecosystem restoration. Here we use 2455 experimental crosses between 12 population pairs of the rare perennial plant Rutidosis leptorrhynchoides (Asteraceae) to investigate the multi-generational (F₁, F₂, F₃) fitness outcomes of inter-population hybridization. We detected no evidence of outbreeding depression, with inter-population hybrids and backcrosses showing either similar fitness or significant heterosis for fitness components across the three generations. Variation in heterosis among population pairs was best explained by characteristics of the foreign source or home population, and was greatest when the source population was large, with high genetic diversity and low inbreeding, and the home population was small and inbred. Our results indicate that the primary consideration for maximizing progeny fitness following population augmentation or restoration is the use of seed from large, genetically diverse populations.     

Demographic factors and genetic variation influence population persistence under environmental change

Population persistence has been studied in a conservation context to predict the fate of small or declining populations. Persistence models have explored effects on extinction of random demographic and environmental fluctuations, but in the face of directional environmental change they should also integrate factors affecting whether a population can adapt. Here, we examine the population‐size dependence of demographic and genetic factors and their likely contributions to extinction time under scenarios of environmental change. Parameter estimates were derived from experimental populations of the rainforest species, Drosophila birchii, held in the lab for 10 generations at census sizes of 20, 100 and 1000, and later exposed to five generations of heat‐knockdown selection. Under a model of directional change in the thermal environment, rapid extinction of populations of size 20 was caused by a combination of low growth rate (r) and high stochasticity in r. Populations of 100 had significantly higher reproductive output, lower stochasticity in r and more additive genetic variance (V_A) than populations of 20, but they were predicted to persist less well than the largest size class. Even populations of 1000 persisted only a few hundred generations under realistic estimates of environmental change because of low V_A for heat‐knockdown resistance. The experimental results document population‐size dependence of demographic and adaptability factors. The simulations illustrate a threshold influence of demographic factors on population persistence, while genetic variance has a more elastic impact on persistence under environmental change.     

Demographic and genetic estimates of effective population size (Ne) reveals genetic compensation in steelhead trout

Estimates of effective population size (Ne) are required to predict the impacts of genetic drift and inbreeding on the evolutionary dynamics of populations. How the ratio of Ne to the number of sexually mature adults (N) varies in natural vertebrate populations has not been addressed. We examined the sensitivity of Ne/N to fluctuations of N and determined the major variables responsible for changing the ratio over a period of 17 years in a population of steelhead trout (Oncorhynchus mykiss) from Washington State. Demographic and genetic methods were used to estimate Ne. Genetic estimates of Ne were gained via temporal and linkage disequilibrium methods using data from eight microsatellite loci. DNA for genetic analysis was amplified from archived smolt scales. The Ne/N from 1977 to 1994, estimated using the temporal method, was 0.73 and the comprehensive demographic estimate of Ne/N over the same time period was 0.53. Demographic estimates of Ne indicated that variance in reproductive success had the most substantial impact on reducing Ne in this population, followed by fluctuations in population size. We found increased Ne/N ratios at low N, which we identified as genetic compensation. Combining the information from the demographic and genetic methods of estimating Ne allowed us to determine that a reduction in variance in reproductive success must be responsible for this compensation effect. Understanding genetic compensation in natural populations will be valuable for predicting the effects of changes in N (i.e. periods of high population density and bottlenecks) on the fitness and genetic variation of natural populations.     

Low genetic variation reduces cross-compatibility and offspring fitness in populations of a narrow endemic plant with a self-incompatibility system

Genetic variation was shown earlier to bereduced in smaller populations of the narrowendemic putatively self-incompatible Cochlearia bavarica. To test whether thisnegatively affects plant fitness by reducedavailability of compatible mates and byinbreeding depression, we studied effects ofpopulation size and pollination treatments oncross-compatibility and offspring fitness in 16isolated populations of this plant. After openpollination, compatibility of crosses (i.e.,whether at least one fruit developed per markedflower), fruit set of compatible crosses, andcumulative fitness (number of plants permaternal ovule) after 14 months in a commongarden were lower for plants from smallerpopulations. Throughout the study, cumulativefitness was lower after hand pollination withpollen of one donor than after open pollination(finally 73.4% lower), suggesting that severalpollen donors or single pollen donors of higherquality are involved in open pollination.Moreover, cumulative fitness was lower afterhand selfing than after hand outcrossing(finally 69.4% lower), indicating bothinbreeding depression and reduced compatibilityafter selfing. High self-compatibility(40.6%), dry stigmas, and differences in thecompatibility of 11 of 33 experimentalreciprocal crosses between plant pairsconfirmed that C. bavarica has asporophytic self-incompatibility system, as iscommon in the Brassicaceae. Our studydemonstrates, that plants in smallerpopulations of species with a sporophyticself-incompatibility system can experiencetwofold fitness reductions associated withreduced genetic variability, i.e., twofoldgenetic Allee effects: via reducedcross-compatibility and via reduced offspringfitness.     

Offspring fitness in relation to population size and genetic variation in the rare perennial plant species Gentiana pneumonanthe (Gentianaceae)

Seeds were sampled from 19 populations of the rare Gentiana pneumonanthe, ranging in size from 5 to more than 50,000 flowering plants. An analysis was made of variation in a number of life-history characters in relation to population size and offspring heterozygosity (based on seven polymorphic isozyme loci). Life-his-tory characters included seed weight, germination rate, proportion of seeds germinating, seedling mortality, seedling weight, adult weight, flower production per plant and proportion of plants flowering per family. Principal component analysis (PCA) reduced the dataset to three main fitness components. The first component was highly correlated with adult weight and flowering performance, the second with germination performance and the third component with seed and seedling weight and seedling mortality. The latter two components were considered as being maternally influenced, since these comprised life-history traits that were significantly correlated with seed weight. Multiple regression analysis showed that variation in the first fitness component was mainly associated with heterozygosity and not with population size, while the third fitness component was only correlated with population size and not with heterozygosity. The latter relationship appeared to be non-linear, which suggests a stronger loss of fitness in the smallest populations. The second (germination) component was neither correlated with population size nor with genetic variation. There was only a weak association between population size, heterozygosity and the population coefficients of variation for each life history character. Most correlation coefficients were negative, however, which suggests that there is more variation among progeny from smaller populations. We conclude that progeny from small populations of Gentiana pneumonanthe show reduced fitness and may be phenotypically more variable. One of the possible causes of the loss of fitness is a combination of unfavourable environmental circumstances for maternal plants in small populations and increased inbreeding. The higher phenotypic variation in small populations may also be a result of inbreeding, which can lead to deviation of individuals from the average phenotype through a loss of developmental stability.     

Temporal variation in genetic diversity and effective population size of Mediterranean and subalpine Arabidopsis thaliana populations

Currently, there exists a limited knowledge on the extent of temporal variation in population genetic parameters of natural populations. Here, we study the extent of temporal variation in population genetics by genotyping 151 genome-wide SNP markers polymorphic in 466 individuals collected from nine populations of the annual plant Arabidopsis thaliana during 4 years. Populations are located along an altitudinal climatic gradient from Mediterranean to subalpine environments in NE Spain, which has been shown to influence key demographic attributes and life cycle adaptations. Genetically, A. thaliana populations were more variable across space than over time. Common multilocus genotypes were detected several years in the same population, whereas low-frequency multilocus genotypes appeared only 1 year. High-elevation populations were genetically poorer and more variable over time than low-elevation populations, which might be caused by a higher overall demographic instability at higher altitudes. Estimated effective population sizes were low but also showed a significant decreasing trend with increasing altitude, suggesting a deeper impact of genetic drift at high-elevation populations. In comparison with single-year samplings, repeated genotyping over time captured substantially higher amount of genetic variation contained in A. thaliana populations. Furthermore, repeated genotyping of populations provided novel information on the genetic properties of A. thaliana populations and allowed hypothesizing on their underlying mechanisms. Therefore, including temporal genotyping programmes into traditional population genetic studies can significantly increase our understanding of the dynamics of natural populations.     

Mating system and genetic variation in the endangered New Zealand takahe

The takahe (Porphyrio hochstetteri) is ahighly endangered flightless rail that isendemic to New Zealand. Only one remnantpopulation of takahe (120 adults) is left inthe wild in Fiordland, which has been thesource for introductions to four predator-freeislands. The objective of the present studywas to determine the mating system andamount of genetic variation in takahe usingmultilocus DNA profiling, in order to assist inthe management of the island populations. There was no evidence of extra-pair paternityfor the 27 (73%, n = 37) offspring towhich paternity could be resolved. Thepaternity of the remaining 10 offspring couldnot be resolved due to low levels ofminisatellite DNA variation, but in none wasthe resident male excluded. Overall, the DNAresults along with behavioral and life historyinformation indicate that extra-pairfertilizations should be rare or absent, andtakahe join a small but growing list oflong-lived species of birds that have beenshown to exhibit genetic monogamy. Inaddition, the levels of minisatellite DNAvariation detected in takahe are low relativeto those reported for most other known outbredavian populations, and are consistent with theevidence of the takahe's persistence as asmall, isolated population in Fiordland over atleast the last 100 years. The low geneticvariation is discussed in relation to possibleevidence of environment depended inbreedingdepression in translocated island populationsof takahe.     

An empirical test of the estimation of historical effective population size using Drosophila melanogaster

The availability of a large number of high-density markers (SNPs) allows the estimation of historical effective population size (N_e) from linkage disequilibrium between loci. A recent refinement of methods to estimate historical N_e from the recent past has been shown to be rather accurate with simulation data. The method has also been applied to real data for numerous species. However, the simulation data cannot encompass all the complexities of real genomes, and the performance of any estimation method with real data is always uncertain, as the true demography of the populations is not known. Here, we carried out an experimental design with Drosophila melanogaster to test the method with real data following a known demographic history. We used a population maintained in the laboratory with a constant census size of about 2800 individuals and subjected the population to a drastic decline to a size of 100 individuals. After a few generations, the population was expanded back to the previous size and after a few further generations again expanded to twice the initial size. Estimates of historical N_e were obtained with the software GONE both for autosomal and X chromosomes from samples of 17 individuals sequenced for the whole genome. Estimates of the historical effective size were able to infer the patterns of changes that occurred in the populations showing generally good performance of the method. We discuss the limitations of the method and the application of the software carried out so far.