Bottlenecked but long-lived: high genetic diversity retained in white-tailed eagles upon recovery from population decline

Most of the white-tailed eagle (Haliaeetus albicilla) populations in Europe experienced dramatic declines during the twentieth century. However, owing to intense conservation actions and the ban of DDT and other persistent pollutants, populations are currently recovering. We show that despite passing through demographic bottlenecks, white-tailed eagle populations have retained significant levels of genetic diversity. Both genetic and ringing data indicate that migration between populations has not been a major factor for the maintenance of genetic variability. We argue that the long generation time of eagles has acted as an intrinsic buffer against loss of genetic diversity, leading to a shorter effective time of the experienced bottleneck. Notably, conservation actions taken in several small sub-populations have ensured the preservation of a larger proportion of the total genetic diversity than if conservation had focused on the population stronghold in Norway. For conservation programmes targeting other endangered, long-lived species, our results highlight the possibility for local retention of high genetic diversity in isolated remnant populations.     

Attitudes toward genetic testing among the general population and relatives of patients with a severe genetic disease: a survey from Finland.

In the present study we explore the attitudes of the Finnish population toward genetic testing by conducting a questionnaire study of a stratified sample of the population as well as of family members of patients with a severe hereditary disease, aspartylglucosaminuria (AGU). The questionnaire evaluated attitudes toward gene tests in general and also respondents' preparedness to undergo gene tests for predictive testing, carrier detection, prenatal diagnosis, and selective abortion, in theoretical situations. The results of the study indicate that both the Finnish population in general and family members of AGU patients have a favorable attitude toward genetic testing. However, a commonly expressed reason against testing was that test results might lead to discrimination in employment or insurance policies. Based on the responses, we predict that future genetic testing programs will most probably be met with a high acceptance rate by the Finnish population.     

Estimation of population divergence times from non-overlapping genomic sequences: examples from dogs and wolves

Despite recent technological advances in DNA sequencing, incomplete coverage remains to be an issue in population genomics, in particular for studies that include ancient samples. Here, we describe an approach to estimate population divergence times for non-overlapping sequence data that is based on probabilities of different genealogical topologies under a structured coalescent model. We show that the approach can be adapted to accommodate common problems such as sequencing errors and postmortem nucleotide misincorporations, and we use simulations to investigate biases involved with estimating genealogical topologies from empirical data. The approach relies on three reference genomes and should be particularly useful for future analysis of genomic data that comprise of nonoverlapping sets of sequences, potentially from different points in time. We applied the method to shotgun sequence data from an ancient wolf together with extant dogs and wolves and found striking resemblance to previously described fine-scale population structure among dog breeds. When comparing modern dogs to four geographically distinct wolves, we find that the divergence time between dogs and an Indian wolf is smallest, followed by the divergence times to a Chinese wolf and a Spanish wolf, and a relatively long divergence time to an Alaskan wolf, suggesting that the origin of modern dogs is somewhere in Eurasia, potentially southern Asia. We find that less than two-thirds of all loci in the boxer and poodle genomes are more similar to each other than to a modern gray wolf and that--assuming complete isolation without gene flow--the divergence time between gray wolves and modern European dogs extends to 3,500 generations before the present, corresponding to approximately 10,000 years ago (95% confidence interval [CI]: 9,000-13,000). We explicitly study the effect of gene flow between dogs and wolves on our estimates and show that a low rate of gene flow is compatible with an even earlier domestication date ～30,000 years ago (95% CI: 15,000-90,000). This observation is in agreement with recent archaeological findings and indicates that human behavior necessary for domestication of wild animals could have appeared much earlier than the development of agriculture.     

A cautionary tale on genetic screens based on a gain-of-expression approach: The case of LanB1

Gain of function screens have being frequently used to search for genes affecting a particular adult character or developmental process. These experiments are made possible by the adoption of the Gal4/UAS system to flies, and by the design of P elements bearing UAS sequences. We recently published two screens in which a large number of newly generated P-UAS insertions were crossed with Gal4 drivers expressed in the pupal veins and in the central region of the wing disc. From the data obtained in these and other screens, it seems that a gain-of-function phenotype is a rare occurrence observed only for about 5–8% of insertion sites. Insertions affecting the expression of signaling molecules were particularly enriched in the screens. In contrast, gain-of-function phenotypes due to insertions not belonging to this class appear to be caused by multiple protein-specific mechanisms that could only be unraveled after extensive analysis. We present some data concerning the overexpression of LamB1, a gene encoding the B subunit of Laminin trimers in Drosophila, and show that Notch protein subcellular localization and signaling is compromised in cells overexpressing LanB1.     

The hunting of migratory birds in Europe: a ringing recovery analysis

The hunting of 20 species of migratory birds in Europe and countries bordering the Mediterranean Sea was investigated using ringing recovery data. The intensity of the hunting of birds in each country was measured by the calculation of an index which controls for ringing effort and reporting rates. The hunting of birds was shown to be consistently high in western Mediterranean countries, particularly in southern France, northern and southwestern Iberia, northern Italy and in northwest Africa. Geographical patterns in the relative magnitude of hunting indices for different breeding populations were species-specific. In Europe most birds are taken during autumn and winter but in North Africa hunting is almost equally prevalent in spring. All species investigated, other than those that remain legitimate quarry species, showed a general reduction in index values after 1980. Analysis of long-term trends in index values since 1950 indicated a statistically significant overall decrease in the hunting of the majority of species. These changes are thought to be at least partly attributable to a real decline in the taking of birds but they may also reflect changed attitudes to reporting the hunting of species which are now protected. This analysis provides the first quantitative Europe-wide assessment of geographical and temporal trends in the hunting of migratory birds.     

Limitation of population recovery: a stochastic approach to the case of the emperor penguin

Major population crashes due to natural or human‐induced environmental changes may be followed by recoveries. There is a growing interest in the factors governing recovery, in hopes that they might guide population conservation and management, as well as population recovery following a re‐introduction program. The emperor penguin Aptenodytes forsteri population in Terre Adélie, Antarctica, declined by 50% during a regime shift in the mid‐1970s, when abrupt changes in climate and ocean environment regimes affected the entire Southern Ocean ecosystem. Since then the population has remained stable and has not recovered. To determine the factors limiting recovery, we examined the consequences of changes in survival and breeding success after the regime shift. Adult survival recovered to its pre‐regime shift level, but the mean breeding success declined and the variance in breeding success increased after the regime shift. Using stochastic matrix population models, we found that if the distribution of breeding success observed prior to the regime shift had been retained, the emperor penguin population would have recovered, with a median time to recovery of 36 years. The observed distribution of breeding success after the regime shift makes recovery very unlikely. This indicates that the pattern of breeding success is sufficient to have prevented emperor penguin population recovery. The population trajectory predicted on the basis of breeding success agrees with the observed trajectory. This suggests that the net effect of any facors other than breeding success must be small. We found that the probability of recovery and the time to recovery depend on both the mean and variance of breeding success. Increased variance in breeding success increases the probability of recovery when mean success is low, but has the opposite effect when the mean is high. This study shows the important role of breeding success in determining population recovery for a long‐lived species and demonstrates that demographic mechanisms causing population crash can be different from those preventing population recovery.     

Successful maintenance of a stingless bee population despite a severe genetic bottleneck

Stingless bees play an important ecological role as pollinators of many wild plant species in the tropics and have significant potential for the pollination of agricultural crops. Nevertheless, conservation efforts as well as commercial breeding programmes require better guidelines on the amount of genetic variation that is needed to maintain viable populations. In this context, we carried out a long-term genetic study on the stingless bee Melipona scutellaris to evaluate the population viability consequences of prolonged breeding from a small number of founder colonies. In particular, it was artificially imposed a genetic bottleneck by setting up a population starting from only two founder colonies, and continued breeding from it for a period of over 10?years in a location outside its natural area of occurrence. We show that despite a great reduction in the number of alleles present at both neutral microsatellite loci and the sex-determining locus relative to its natural source population, and an increased frequency in the production of sterile diploid males, the genetically impoverished population could be successfully bred and maintained for at least 10?years. This shows that in stingless bees, breeding from a small stock of colonies may have less severe consequences than previously suspected. In addition, we provide a simulation model to determine the number of colonies that are needed to maintain a certain number of sex alleles in a population, thereby providing useful guidelines for stingless bee breeding and conservation efforts.     

Inferring population decline and expansion from microsatellite data: a simulation-based evaluation of the Msvar method

Reconstructing the demographic history of populations is a central issue in evolutionary biology. Using likelihood-based methods coupled with Monte Carlo simulations, it is now possible to reconstruct past changes in population size from genetic data. Using simulated data sets under various demographic scenarios, we evaluate the statistical performance of Msvar, a full-likelihood Bayesian method that infers past demographic change from microsatellite data. Our simulation tests show that Msvar is very efficient at detecting population declines and expansions, provided the event is neither too weak nor too recent. We further show that Msvar outperforms two moment-based methods (the M-ratio test and Bottleneck) for detecting population size changes, whatever the time and the severity of the event. The same trend emerges from a compilation of empirical studies. The latest version of Msvar provides estimates of the current and the ancestral population size and the time since the population started changing in size. We show that, in the absence of prior knowledge, Msvar provides little information on the mutation rate, which results in biased estimates and/or wide credibility intervals for each of the demographic parameters. However, scaling the population size parameters with the mutation rate and scaling the time with current population size, as coalescent theory requires, significantly improves the quality of the estimates for contraction but not for expansion scenarios. Finally, our results suggest that Msvar is robust to moderate departures from a strict stepwise mutation model.     

Sex ratio of leopards taken in trophy hunting: genetic data from Tanzania

The sex ratio of leopards, Panthera pardus, taken by trophyhunters in Tanzania is examined. We used sex specific molecularmarkers to analyze 77 samples collected from animals shot betweenthe years 1995–1998 and found that 28.6% were females, despitethe fact that only males are allowed on licenses and all skinswere tagged as males. The model used for quota setting assumesthat only males are shot, but the effect of this violation ofquotas is unknown. Off-take in Tanzania does not currently fillquotas, but when off-take approach maximum levels, compliancewith set quotas and regulations will be critical for sustainableharvest.     

Parasite invasion following host reintroduction: a case study of Yellowstone's wolves

Wildlife reintroductions select or treat individuals for good health with the expectation that these individuals will fare better than infected animals. However, these individuals, new to their environment, may also be particularly susceptible to circulating infections and this may result in high morbidity and mortality, potentially jeopardizing the goals of recovery. Here, using the reintroduction of the grey wolf (Canis lupus) into Yellowstone National Park as a case study, we address the question of how parasites invade a reintroduced population and consider the impact of these invasions on population performance. We find that several viral parasites rapidly invaded the population inside the park, likely via spillover from resident canid species, and we contrast these with the slower invasion of sarcoptic mange, caused by the mite Sarcoptes scabiei. The spatio-temporal patterns of mange invasion were largely consistent with patterns of host connectivity and density, and we demonstrate that the area of highest resource quality, supporting the greatest density of wolves, is also the region that appears most susceptible to repeated disease invasion and parasite-induced declines. The success of wolf reintroduction appears not to have been jeopardized by infectious disease, but now shows signs of regulation or limitation modulated by parasites.     

Influence of population decline, fishing, and spawner variability on the recovery of marine fishes

Based on an analysis of 90 marine fish populations, collapses (the greatest proportional reduction in spawner biomass over 15 years) are predicated typically by dramatic increases in fishing mortality and recoveries are more likely to occur when exploitation is reduced. However, among populations for which fishing mortality declined after collapse, recovery was independent of exploitation rate, even when fishing mortality (F) post-collapse was expressed as a function of each population's maximum growth rate (r). After a period of 15 years, many populations that experienced 15 year declines >60% exhibited little or no recovery, despite considerable reductions in fishing mortality. This suggests that factors other than fishing may be considerably more important to recovery, and fishing less important, than previously thought. Furthermore, among populations for which fishing mortality decreased post-collapse, rate of population decline was a reliable predictor of recovery. With the possible exception of clupeids, variation in marine fish breeding population size was found to differ little from that of other vertebrates, and such variability appears to have no effect on rate of recovery. In addition to providing an empirical framework for the study of population collapse and recovery, the analyses presented here provide a means of assessing the precautionary nature of various population-decline thresholds used to assign extinction risks to marine fish.     

Illegal hunting and law enforcement during a period of economic decline in Zimbabwe: A case study of northern Gonarezhou National Park and adjacent areas

Illegal hunting of wildlife, or top-down harvesting, is a major issue in today's society, particularly in tropical ecosystems. There has been widespread concern about increasing illegal hunting of wildlife in most conservation areas in Zimbabwe following the political instability and economic decline the country faced since 2000. In this study, we focused on the northern Gonarezhou National Park (GNP), a large and unfenced protected area, and adjacent communal areas in southern Zimbabwe. We hypothesised that illegal hunting activities would (1) be perceived to have increased due to economic collapse and (2) vary with law enforcement efforts. A total of 236 local residents from eight villages adjacent to the northern GNP were interviewed using semi-structured questionnaires from December 2010 to May 2011, and law enforcement data for northern GNP between 2000 and 2010 were retrieved from the park law enforcement database. A total of 26 animal species were reportedly hunted. Bushmeat consumption and the need for local trade to raise income were reported as the main reasons behind illegal hunting. Contrary to the first hypothesis, the majority of respondents (n = 156, 66%) reported that illegal hunting activities had declined between 2000 and 2010 largely due to increased park protection as also supported by law enforcement data. A total of 22 animal species were recorded as having been illegally hunted in northern GNP. The number of illegal hunters arrested declined with increased law enforcement efforts although the number of wire snares recovered and hunting dogs shot appeared to increase following increased law enforcement efforts. These results partly support the second hypothesis that illegal hunting activities would vary with law enforcement efforts.     

Inferring sex-biased dispersal from population genetic tools: a review

Sex-biased dispersal, where individuals of one sex stay or return to their natal site (or group) to breed while individuals of the other sex are prone to disperse, is a wide-spread pattern in vertebrate organisms. In general, mammals exhibit male-biased dispersal whereas birds exhibit female-bias. Dispersal estimates are often difficult to obtain from direct field observations. Here we describe different methods for inferring sex-specific dispersal using population genetic tools and discuss the problems they can raise. We distinguish two types of methods: those based on bi-parental markers (eg comparison of male/female relatedness, F(st) and assignment probabilities) and those relying on the comparison between markers with different modes of inheritance (eg mtDNA markers and microsatellites). Finally, we discuss statistical problems that are encountered with these different methods (eg pseudoreplication, problems due to the comparison of distinct markers). While the genetic methods to detect sex-biased dispersal are now relatively well developed, their interpretation can prove problematic due to the confounding effects of factors such as the mating system of the species. Moreover, the relative power of these methods is not well known and requires further investigation.     

When hunting benefits raptors: a case study of game species and vultures

Management of hunting activity to serve as a tool for sustainable development has become a key issue in conservation biology. However, little evidence is available showing positive impacts of hunting on ecosystem conservation, limiting its capability to be used as a conservation tool. We analysed hunting and its positive influence on the ecology and conservation of the griffon vulture (Gyps fulvus), a scavenger with a relevant function in the ecosystem, in the Cantabrian Mountains, NW Spain. Use of the area by vultures was addressed by looking for cliffs used as roosts or colonies, and consumption of game species by vultures was evaluated through field surveys and questionnaires to hunters. Results revealed a strong spatiotemporal adjustment in the use of the area by vultures and hunting events, especially of red deer and wild boar. Vultures occupied roosting sites very close to the main hunting sectors of these game species and often were seen consuming their carcasses. The spatiotemporal pattern of roost use by vultures strongly overlapped with hunting of red deer. The numbers of both red deer and wild boar hunting episodes within 3.5 km around the roosts were the best predictors of vulture occurrence and number. Our estimates show that hunting could feed around 1,800 vultures/6 months. Hunting can thus influence species at the top of the ecosystem (scavengers) and could aid sustainable management of griffon vulture populations, reconciling hunting and conservation. However, negative and positive impacts should be taken into account simultaneously for an overall evaluation of hunting on ecosystem conservation.     

Structuring the genetic heterogeneity of the Basque population: a view from classical polymorphisms

In this study we analyze 18 classical polymorphisms (ABO, Rh, MNSs, Lewis, P, Duffy, Kell, ADA, ESD, PGM1, PGD, AK1, ACP1, GLO1, HP, GC, TF, and PI) in over 2000 autochthonous individuals from 14 natural districts in three provinces of the Basque Country (Alava, Guipuzcoa, and Biscay). Heterogeneity analysis via the chi2 test and a calculation of F(ST) indicate that there is significant genetic heterogeneity between the Basque districts. The R matrix informs us that this heterogeneity is not significantly concentrated in a single district or in the districts of a single province, but is rather distributed among several districts belonging to the three provinces analyzed. We undertake to assess the influence of various historical, geographical, and cultural factors on the genetic structure of the Basque population. Analysis suggests that allele distribution is geographically patterned in the Basque Country. The gradient distributions observed in the case of some alleles (ABO*O, RH*cDE, RH*cde, MNS*MS, and ACP1*C) on the basis of Moran's autocorrelation coefficient I, along with the influence of the two main travel routes through the Basque Country (western route through Bilbao and eastern route through Vitoria), suggest that the gene flow tends toward the coast. As regards other factors considered (administrative division, repopulation processes, linguistic heterogeneity, and north vs. south cultural heterogeneity), we detected only a certain influence exerted by an old tribal differentiation (2000 B.P.), which would diminish with the passage of time.     

Perfect simulation from nonneutral population genetic models: variable population size and population subdivision

We show how the idea of monotone coupling from the past can produce simple algorithms for simulating samples at a nonneutral locus under a range of demographic models. We specifically consider a biallelic locus and either a general variable population size mode or a general migration model for population subdivision. We investigate the effect of demography on the efficacy of selection and the effect of selection on genetic divergence between populations.     

Human influence on the population decline and loss of genetic diversity in a small and isolated population of Sichuan snub-nosed monkeys (Rhinopithecus roxellana)

Human activities have caused worldwide loss and fragmentation of natural habitats, resulting in the decline and isolation of wild populations, consequently increasing their risks of extinctions. We investigated the genetic consequences of anthropogenic effects on the Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in the Shennongjia Nature Reserve (SNR), which is a small and isolated distribution of R. roxellana in China and would continue to be threatened by habitat degradation and loss, using extensive sampling and 16 microsatellite loci. High level of genetic variation was observed from 202 individuals collected from three R. roxellana populations (SNR population, Sichuan-Gansu population and Shaanxi population). However, R. roxellana in SNR showed the lowest genetic diversity. The likelihood analysis of migration/drift equilibrium indicated that the SNR population suffered much stronger effect of drift than the other two populations, indicating that small populations are prone to be affected by drift. The STRUCTURE analysis identified two clusters, separating the SNR population from the other two populations, suggesting an increasing drift-induced differentiation between SNR and the other two populations. Bottleneck tests revealed that R. roxellana in SNR experienced a severe population decline (37-fold) during the past 500?years as a consequence of human population expansion. The current effective population size (Ne) in SNR is less than 100 and the ratio of Ne to the census population size is approximately 0.08. Based on our findings, we suggest that the SNR population should be monitored systematically and considered as an important conservation and management unit.     

Conservation genetics of American Dipper (<Emphasis Type="Italic">Cinclus mexicanus</Emphasis>): the genetic status of a population in severe decline

American Dippers (Cinclus mexicanus) were once known to occur in streams throughout the Black Hills of South Dakota and Wyoming, but now dippers number about 50–75 individuals and reside almost exclusively in a single stream. The recent decline of the American Dipper in the Black Hills of South Dakota is thought to be due to local stream degradation. As a result of the decline of C. mexicanus in the Black Hills of South Dakota and Wyoming, the Black Hills population of American Dippers is a candidate for designation as a distinct population segement (DPS) and might warrant protection and special management. One criterion for DPS designation is genetic uniqueness. Here we present the results of a genetic assessment of the Black Hills population of C. mexicanus. Data presented here indicate that the dipper population in the Black Hills is genetically distinct from other sampled populations. Further population sampling will be needed to understand the genetic population structure of C. mexicanus throughout its range. Furthermore, the recent decline in the Black Hills dipper population should be a warning that other populations (and other species) may be experiencing similar declines and that such montane habitats are worthy of special management.     

Evidence that disease-induced population decline changes genetic structure and alters dispersal patterns in the Tasmanian devil

Infectious disease has been shown to be a major cause of population declines in wild animals. However, there remains little empirical evidence on the genetic consequences of disease-mediated population declines, or how such perturbations might affect demographic processes such as dispersal. Devil facial tumour disease (DFTD) has resulted in the rapid decline of the Tasmanian devil, Sarcophilus harrisii, and threatens to cause extinction. Using 10 microsatellite DNA markers, we compared genetic diversity and structure before and after DFTD outbreaks in three Tasmanian devil populations to assess the genetic consequences of disease-induced population decline. We also used both genetic and demographic data to investigate dispersal patterns in Tasmanian devils along the east coast of Tasmania. We observed a significant increase in inbreeding (F_IS pre/post-disease −0.030/0.012, P<0.05; relatedness pre/post-disease 0.011/0.038, P=0.06) in devil populations after just 2–3 generations of disease arrival, but no detectable change in genetic diversity. Furthermore, although there was no subdivision apparent among pre-disease populations (θ=0.005, 95% confidence interval (CI) −0.003 to 0.017), we found significant genetic differentiation among populations post-disease (θ=0.020, 0.010–0.027), apparently driven by a combination of selection and altered dispersal patterns of females in disease-affected populations. We also show that dispersal is male-biased in devils and that dispersal distances follow a typical leptokurtic distribution. Our results show that disease can result in genetic and demographic changes in host populations over few generations and short time scales. Ongoing management of Tasmanian devils must now attempt to maintain genetic variability in this species through actions designed to reverse the detrimental effects of inbreeding and subdivision in disease-affected populations.