Heterozygosity-fitness correlations in a bottlenecked island species: a case study on the Seychelles warbler

We used capture-mark-recapture models to investigate the effects of both individual and parental heterozygosity, measured at microsatellite loci on the survival of Seychelles warblers (Acrocephalus sechellensis), an endemic island species which went through a severe population bottleneck in the middle of the last century. We found that an individual's survival was not correlated with multilocus heterozygosity, or with heterozygosity at any specific locus. However, maternal, but not paternal, multilocus heterozygosity was positively associated with offspring survival, but only in years with low survival probabilities. A nestling cross-fostering experiment showed that this was a direct maternal effect as there was an effect of the genetic mother's, but not of the social mother's, heterozygosity. Heterozygosity-fitness correlations at microsatellite markers were generally assumed to reflect genome-wide effects. Although this might be true in partially inbred populations, such correlations may also arise as a result of local effects with specific markers being closely linked to genes which determine fitness. However, heterozygosity at the individual microsatellite loci was not correlated and therefore does not seem to reflect genome-wide heterozygosity. This suggests that even in a small bottlenecked population, heterozygosity-fitness correlations may not be caused by genome-wide effects. Support for the local effects hypothesis was also equivocal; although three specific loci were associated with offspring survival, including all single-locus heterozygosities as independent predictors for the variation in survival was not supported by the data. Furthermore, in contrast to the local effects hypothesis, the loci which contributed most to the heterozygosity-survival relationship were not more polymorphic than the other loci. This study highlights the difficulties in distinguishing between the two hypotheses.     

Age-specific effect of heterozygosity on survival in alpine marmots, Marmota marmota

The fitness consequences of heterozygosity and the mechanisms underpinning them are still highly controversial. Using capture–mark–recapture models, we investigated the effects of individual heterozygosity, measured at 16 microsatellite markers, on age-dependent survival and access to dominance in a socially monogamous mammalian species, the alpine marmot. We found a positive correlation between standardized multilocus heterozygosity and juvenile survival. However, there was no correlation between standardized multilocus heterozygosity and either survival of older individuals or access to dominance. The disappearance of a significant heterozygosity fitness correlation when individuals older than juveniles are considered is consistent with the prediction that differences in survival among individuals are maximal early in life. The lack of a correlation between heterozygosity and access to dominance may be a consequence of few homozygous individuals attaining the age at which they might reach dominance. Two hypotheses have been proposed to explain heterozygosity-fitness correlations: genome-wide effects reflected by all markers or local effects of specific markers linked to genes that determine fitness. In accordance with genome-wide effects of heterozygosity, we found significant correlations between heterozygosities calculated across single locus or across two sets of eight loci. Thus, the genome-wide heterozygosity effect seems to explain the observed heterozygosity-fitness correlation in the alpine marmot.     

Effective population sizes and migration rates in fragmented populations of an endangered insect (Coenagrion mercuriale: Odonata)

1. Effective population sizes (N(e)) and migration rates (m) are critical evolutionary parameters that impact on population survival and determine the relative influence of selection and genetic drift. While the parameter m is well-studied in animal populations, N(e) remains challenging to measure and consequently is only rarely estimated, particularly in insect taxa. 2. We used demographic and genetic methods to estimate N(e) and m in a fragmented population of the endangered damselfly Coenagrion mercuriale to better understand the contrast between genetic and field estimates of these parameters and also to identify the spatial scale over which populations may become locally adapted. 3. We found a contrast between demographic- and genetic-based estimates of these parameters, with the former apparently providing overestimates of N(e), owing to substantial underestimation of the variance in reproductive success, and the latter overestimating m, because spatial genetic structure is weak. 4. The overall N(e) of sites within the population network at Beaulieu Heath, the largest C. mercuriale site in the UK, was estimated to vary between approximately 60 and 2700. 5. While N(e) was not correlated with either the total numbers of adults (N) or the area of habitat, this parameter was always less than N, because of substantial variance in reproductive success. The ratio N(e)/N varied between 0.006 and 0.42 and was generally larger in smaller populations, possibly representing some 'genetic compensation'. 6. From a simple genetic model and these data on N(e) and m, it seems that populations of C. mercuriale have the potential to respond to localized spatial variation in selection and this would need to be considered for future genetic management of this endangered species.     

Are extra-pair young better than within-pair young? A comparison of survival and dominance in alpine marmot

1. In socially monogamous species, females may seek extra-pair copulation to gain genetic benefits. In order to test this 'genetic quality' hypothesis, one must compare the performance of extra-pair young (EPY) and within-pair young (WPY). Such tests, however, are scarce and results published so far are inconclusive. 2. Here, we test the 'genetic quality' hypothesis using multistate capture-recapture models to compare age-specific survival and access to dominance between EPY and WPY in the alpine marmot Marmota marmota, a socially monogamous mammal showing extra-pair paternities. 3. When compared with WPY, survival of EPY was higher by 15%, 10% and 30%, for juveniles, yearlings and 2-year-old individuals, respectively. Survival at older ages did not differ. 4. Survival corresponded to true survival for yearlings and juveniles as dispersal does not occur before 2 years of age in marmots. For older individuals, survival estimates included a mixture of survival and dispersal. The 30% increase of the 2-year-old EPY survival might reflect delayed dispersal rather than high survival of EPY as compared with WPY. 5. WPY and EPY had the same probability (0.28) to access dominance at 2 years of age, but EPY were more successful at older ages than WPY (0.46 vs. 0.10). 6. Both survival and reproductive performance were higher in EPY than in WPY. The fitness advantages of adopting such a mixed mating tactic are thus likely to be high for marmot females. We suggest that obtaining genetic benefits is the main evolutionary force driving extra-pair paternity in alpine marmots.     

Recruitment to a seabird population depends on environmental factors and on population size

1. A novel capture-mark-recapture (CMR) method was used to build a multistate model of recruitment by young birds to a breeding population of common guillemots Uria aalge on the Isle of May, Scotland. Recruitment of a total of 2757 individually marked guillemots over 17 years was modelled as a process where individuals had to move from an unobservable state at sea, through a nonbreeding state present in the colony, to the breeding state. The probabilities of individuals returning to the colony in a given year, at age 2 and 3-4 years, were positively correlated with an environmental covariate, the winter North Atlantic Oscillation index (WNAO) in the previous years. 2. For 2 year olds, there was a negative relationship with breeding population size, suggesting that density dependence operated in this colony through limitation of food or some other resource. 3. Survival over the first 2 years of life varied with cohort, but was unrelated to the WNAO. Mean survival over this 2-year period was high at 0.576 (95% CI: 0.444; 0.708). 4. This high survival, combined with a low 'local' survival after age 5 years of 0.695 (0-654; 0.733) and observations of Isle of May chicks at other colonies, suggests that most surviving chicks return to the natal colony before deciding whether to recruit there or move elsewhere.     

The demographic impact of extreme events: stochastic weather drives survival and population dynamics in a long-lived seabird

1. Most scenarios for future climate change predict increased variability and thus increased frequency of extreme weather events. To predict impacts of climate change on wild populations, we need to understand whether this translates into increased variability in demographic parameters, which would lead to reduced population growth rates even without a change in mean parameter values. This requires robust estimates of temporal process variance, for example in survival, and identification of weather covariates linked to interannual variability. 2. The European shag Phalacrocorax aristotelis (L.) shows unusually large variability in population size, and large-scale mortality events have been linked to winter gales. We estimated first-year, second-year and adult survival based on 43 years of ringing and dead recovery data from the Isle of May, Scotland, using recent methods to quantify temporal process variance and identify aspects of winter weather linked to survival. 3. Survival was highly variable for all age groups, and for second-year and adult birds process variance declined strongly when the most extreme year was excluded. Survival in these age groups was low in winters with strong onshore winds and high rainfall. Variation in first-year survival was not related to winter weather, and process variance, although high, was less affected by extreme years. A stochastic population model showed that increasing process variance in survival would lead to reduced population growth rate and increasing probability of extinction. 4. As in other cormorants, shag plumage is only partially waterproof, presumably an adaptation to highly efficient underwater foraging. We speculate that this adaptation may make individuals vulnerable to rough winter weather, leading to boom-and-bust dynamics, where rapid population growth under favourable conditions allows recovery from periodic large-scale weather-related mortality. 5. Given that extreme weather events are predicted to become more frequent, species such as shags that are vulnerable to such events are likely to exhibit stronger reductions in population growth than would be expected from changes in mean climate. Vulnerability to extreme events thus needs to be accounted for when predicting the ecological impacts of climate change.     

Compatible genetic and ecological estimates of dispersal rates in insect (Coenagrion mercuriale: Odonata: Zygoptera) populations: analysis of 'neighbourhood size' using a more precise estimator

Genetic and demographic estimates of dispersal are often thought to be inconsistent. In this study, we use the damselfly Coenagrion mercuriale (Odonata: Zygoptera) as a model to evaluate directly the relationship between estimates of dispersal rate measured during capture-mark-recapture fieldwork with those made from the spatial pattern of genetic markers in linear and two-dimensional habitats. We estimate the 'neighbourhood size' (Nb) - the product of the mean axial dispersal rate between parent and offspring and the population density - by a previously described technique, here called the regression method. Because C. mercuriale is less philopatric than species investigated previously by the regression method we evaluate a refined estimator that may be more applicable for relatively mobile species. Results from simulations and empirical data sets reveal that the new estimator performs better under most situations, except when dispersal is very localized relative to population density. Analysis of the C. mercuriale data extends previous results which demonstrated that demographic and genetic estimates of Nb by the regression method are equivalent to within a factor of two at local scales where genetic estimates are less affected by habitat heterogeneity, stochastic processes and/or differential selective regimes. The corollary is that with a little insight into a species' ecology the pattern of spatial genetic structure provides quantitative information on dispersal rates and/or population densities that has real value for conservation management.     

Estimating the effect of inbreeding on survival

Conservation biologists need to be able to estimate reliably the effects of inbreeding on survival, and need to be able to do so with a range of different data types. Kalinowski and Hedrick described a non-linear maximum likelihood estimation procedure for modelling relationships between survivorship and inbreeding. Although their method is useful for illustrating the concepts involved in modelling such relationships, it is only applicable to simple datasets. We illustrate that the parameter estimates generated by Kalinowski and Hedrick's method are easily obtained using generalized linear modelling procedures available in standard statistical packages, and that these offer several advantages even with simple datasets. We suggest procedures that can be used for modelling relationships between survival and inbreeding with more complex data types, including datasets with multiple and ragged encounters, uncertain detection and random effects.     

Cowpox virus infection in natural field vole Microtus agrestis populations: significant negative impacts on survival

1. Cowpox virus is an endemic virus circulating in populations of wild rodents. It has been implicated as a potential cause of population cycles in field voles Microtus agrestis L., in Britain, owing to a delayed density-dependent pattern in prevalence, but its impact on field vole demographic parameters is unknown. This study tests the hypothesis that wild field voles infected with cowpox virus have a lower probability of survival than uninfected individuals. 2. The effect of cowpox virus infection on the probability of an individual surviving to the next month was investigated using longitudinal data collected over 2 years from four grassland sites in Kielder Forest, UK. This effect was also investigated at the population level, by examining whether infection prevalence explained temporal variation in survival rates, once other factors influencing survival had been controlled for. 3. Individuals with a probability of infection, P(I), of 1 at a time when base survival rate was at median levels had a 22.4% lower estimated probability of survival than uninfected individuals, whereas those with a P(I) of 0.5 had a 10.4% lower survival. 4. At the population level, survival rates also decreased with increasing cowpox prevalence, with lower survival rates in months of higher cowpox prevalence. 5. Simple matrix projection models with 28 day time steps and two stages, with 71% of voles experiencing cowpox infection in their second month of life (the average observed seroprevalence at the end of the breeding season) predict a reduction in 28-day population growth rate during the breeding season from lambda = 1.62 to 1.53 for populations with no cowpox infection compared with infected populations. 6. This negative correlation between cowpox virus infection and field vole survival, with its potentially significant effect on population growth rate, is the first for an endemic pathogen in a cyclic population of wild rodents.     

Recruitment and survival of immature seabirds in relation to oil spills and climate variability

1. In long-lived animals with delayed maturity, the non-breeding component of the population may play an important role in buffering the effects of stochastic mortality. Populations of colonial seabirds often consist of more than 50% non-breeders, yet because they spend much of their early life at sea, we understand little about their impact on the demographic process. 2. Using multistate capture-mark-recapture techniques, we analyse a long-term data set of individually identifiable common guillemots, Uria aalge Pont., to assess factors influencing their immature survival and two-stage recruitment process. 3. Analysis of the distribution of ringed common guillemots during the non-breeding season, separated by age classes, revealed that all age classes were potentially at risk from four major oil spills. However, the youngest age class (0-3 years) were far more widely spread than birds 4-6 years old, which were more widely spread than birds aged 6 and over. Therefore the chance of encountering an oil spill was age-dependent. 4. A 2-year compound survival estimate for juvenile guillemots was weakly negatively correlated with winter sea-surface temperature, but was not influenced by oil spills. Non-breeder survival did not vary significantly over time. 5. In years following four oil spills, juvenile recruitment was almost double the value in non-oil-spill years. Recent work from Skomer Island showed a doubling of adult mortality associated with major oil spills, which probably reduced competition at the breeding colony, allowing increased immature recruitment to compensate for these losses. We discuss the implications of compensatory recruitment for assessing the impact of oil pollution incidents.     

A critical look at some widely used estimators in mark-resighting experiments

1. For many species and circumstances, mark-resighting procedures constitute valid alternatives to capture-recapture methods. Indeed, resightings are generally cheaper to acquire than physically recapturing and rehandling the animals, especially when radiotelemetry or other tracking devices are available. 2. In order to estimate population abundance, the joint hypergeometric maximum likelihood estimator, the Minta-Mangel estimator and the Bowden estimator are implemented in noremark, software which has become very popular with biologists in the past decade. 3. In this paper, the basic assumptions regarding these widely applied procedures are delineated and discussed. A simulation study is performed in order to investigate the robustness of the estimators under failure of the assumptions. 4. Theoretical considerations and simulation results motivate the use of the Bowden estimator which, when marks are distributed quite evenly among groups, constitutes the sole reliable method, offering computational simplicity and robustness. On the other hand, if the marks are distributed unevenly, no mark-resighting procedure seems reliable. An application to a case study is considered.