Effective Population Size in Red-Cockaded Woodpeckers: Population and Model Differences

Loss of genetic variability in isolated populations is an important issue for conservation biology. Most studies involve only a single population of a given species and a single method of estimating rate of loss. Here we present analyses for three different Red-cockaded Woodpecker ( Picoides borealis ) populations from different geographic regions. We compare two different models for estimating the expected rate of loss of genetic variability, and test their sensitivity to model parameters. We found that the simpler model (Reed et al. 1988) consistently estimated a greater rate of loss of genetic variability from a population than did the Emigh and Pollak (1979) model. The ratio of effective population size (which describes the expected rate of loss of genetic variability) to breeder population size varied widely among Red-cockaded Woodpecker populations due to geographic variation in demography. For this species, estimates of effective size were extremely sensitive to survival parameters, but not to the probability of breeding or reproductive success. Sensitivity was sufficient that error in estimating survival rates in the field could easily mask true population differences in effective size. Our results indicate that accurate and precise demographic data are prerequisites to determining effective population size for this species using genetic models, and that a single estimate of rate of loss of genetic variability is not valid across populations.     

Relationship of Genetic Variation to Population Size in Wildlife

Genetic diversity is one of three levels of biological diversity requiring conservation. Genetic theory predicts that levels of genetic variation should increase with effective population size. Soulé (1976) compiled the first convincing evidence that levels of genetic variation in wildlife were related to population size, but this issue remains controversial. The hypothesis that genetic variation is related to population size leads to the following predictions: (1) genetic variation within species should be related to population size; (2) genetic variation within species should be related to island size; (3) genetic variation should be related to population size within taxonomic groups; (4) widespread species should have more genetic variation than restricted species; (5) genetic variation in animals should be negatively correlated with body size; (6) genetic variation should be negatively correlated with rate of chromosome evolution; (7) genetic variation across species should be related to population size; (8) vertebrates should have less genetic variation than invertebrates or plants; (9) island populations should have less genetic variation than mainland populations; and (10) endangered species should have less genetic variation than nonendangered species. Empirical observations support all these hypotheses. There can be no doubt that genetic variation is related to population size, as Soulé proposed. Small population size reduces the evolutionary potential of wildlife species.     

Population Viability Analysis for a Small Population of Red-Cockaded Woodpeckers and an Evaluation of Enhancement Strategies

We performed a series of population and pedigree analyses to examine the viability of a small Red-cockaded Woodpecker ( Picoides borealis ) population located at the Savannah River Site, in Barnwell and Aiken counties of South Carolina. The population's existence and future survival are precarious. As few as four individuals, including just one breeding pair, comprised this population in 1985. Now, primarily because of experimental transformation of birds from other areas, the population has increased to 25. As of 1990, genealogy pedigree analysis showed that the respective contribution of 14 founders to the extant population has not been equal. Founder gender equivalents are low (5.4) but could reach 9.2 if poorly-represented founders were to produce offspring. The fraction of founder gene diversity retained in the current population is 0.91. Successful recovery strategies would ensure 95% probability of population survival while maintaining 90% heterozygosity for 200 years. Viability analyses indicated that, depending on relative effects of inbreeding depression and stochastic environmental events, the Savannah River Site population has a 68–100% chance of extinction during this period. Annual translocation into the population of at least three females and two males for a 10-year period will achieve a 96% probability of survival for 200 years. Even with translocation of numerous males and females per year (up to 50 of each), the 90% heterozygosity goal may not be achieved. We discuss recommendations for choosing individuals for translocation logistical constraints on achieving recovery objectives, and limitations of our modeling approach.     

Inbreeding and Loss of Genetic Variation in a Reintroduced Population of Mauritius Kestrel

Abstract:  Many populations have recovered from severe bottlenecks either naturally or through intensive conservation management. In the past, however, few conservation programs have monitored the genetic health of recovering populations. We conducted a conservation genetic assessment of a small, reintroduced population of Mauritius Kestrel ( Falco punctatus ) to determine whether genetic deterioration has occurred since its reintroduction. We used pedigree analysis that partially accounted for individuals of unknown origin to document that (1) inbreeding occurred frequently (2.6% increase per generation; N _eI= 18.9), (2) 25% of breeding pairs were composed of either closely or moderately related individuals, (3) genetic diversity has been lost from the population (1.6% loss per generation; N _eV= 32.1) less rapidly than the corresponding increase in inbreeding, and (4) ignoring the contribution of unknown individuals to a pedigree will bias the metrics derived from that pedigree, ultimately obscuring the prevailing genetic dynamics. The rates of inbreeding and loss of genetic variation in the subpopulation of Mauritius Kestrel we examined were extreme and among the highest yet documented in a wild vertebrate population. Thus, genetic deterioration may affect this population's long-term viability. Remedial conservation strategies are needed to reduce the impact of inbreeding and loss of genetic variation in this species. We suggest that schemes to monitor genetic variation after reintroduction should be an integral component of endangered species recovery programs.     

Genetic Variation and Outcrossing Rate in Relation to Population Size in Gentiana pneumonanthe L

The amount of genetic variation in the rare perennial herb Gentiana pneumonanthe L. was determined to explore its relation to population size. Differences in isozyme variation between maternal plants and their offspring were used to investigate the relationship between population size and outcrossing rate. In 25 populations in The Netherlands, differing in size from 1 to more than 50,000 flowering individuals, 16 allozyme loci were analyzed on leaves of maternal plants and offspring grown in a greenhouse. Population size was significantly positively correlated with the proportion of polymorphic loci, but only marginally with heterozygosity and the mean effective number of alleles. Most of the studied populations were characterized by a complete absence of rare alleles, and F -statistics suggest relatively high levels of genetic differentiation among populations and thus a low level of gene flow. Leaf samples (maternal) were mostly in Hardy-Weinberg equilibrium, while several offspring samples showed an excess of homozygotes, which suggests selection favoring heterozygotes. Because most small populations consist only of adult survivors from formerly larger populations, this may partly explain the absence of a clear relationship between genetic variation of the maternal plants and population size. A significant positive correlation was found between the level of cross-fertilization and population size. From these results, we conclude that, to some degree, small populations have a reduced level of genetic variation, while their present isolation in nature reserves has resulted in a very limited interpopulational gene flow level. At present a higher level of inbreeding in small populations contributes to a further loss of genetic variation and may also result in reduced offspring fitness.     

Genetic Variation for Morphological and Allozyme Variation in Relation to Population Size in Clarkia dudleyana, an Endemic Annual

Abstract: The maintenance of genetic variation within populations is expected to allow species to respond to evolutionary challenges such as selection and environmental stress. Larger populations are generally expected to maintain larger amounts of genetic variation. Although several studies have found a positive relationship between population size and levels of genetic variation for molecular markers such as allozymes, few comparisons have been made between molecular measures of variation and genetic variation that is likely to be ecologically important. Most ecologically important traits require quantitative genetic analyses. I examined the relationship between levels of genetic variation and population size for both allozymes and morphological traits in a California endemic annual plant, Clarkia dudleyana . Levels of genetic variation for allozymes did not show a significant positive relationship with population size. The level of genetic variance for all of the 18 morphological traits exhibited no significant relationship with population size. Further, allozyme heterozygosities were not related to levels of quantitative genetic variation. These results indicate that levels of allozyme variability do not predict levels of genetic variation for morphological traits in C. dudleyana , suggesting that molecular measures of variation, in general, differ from quantitative genetic measures. These results imply that conservation genetic studies should generally focus on aspects other than measuring levels of genetic variation found within populations.     

Unprecedented Low Levels of Genetic Variation and Inbreeding Depression in an Island Population of the Black-Footed Rock-Wallaby

Abstract: It has been argued that demographic and environmental factors will cause small, isolated populations to become extinct before genetic factors have a significant negative impact. Islands provide an ideal opportunity to test this hypothesis because they often support small, isolated populations that are highly vulnerable to extinction. To assess the potential negative impact of isolation and small population size, we compared levels of genetic variation and fitness in island and mainland populations of the black-footed rock-wallaby ( Petrogale lateralis [Marsupialia: Macropodidae]). Our results indicate that the Barrow Island population of P. lateralis has unprecedented low levels of genetic variation (  H _e = 0.053, from 10 microsatellite loci) and suffers from inbreeding depression (reduced female fecundity, skewed sex ratio, increased levels of fluctuating asymmetry). Despite a long period of isolation ( ∼ 1600 generations) and small effective population size (  N _e ∼ 15), demographic and environmental factors have not yet driven this population to extinction. Nevertheless, it has been affected significantly by genetic factors. It has lost most of its genetic variation and become highly inbred (  F _e = 0.91), and it exhibits reduced fitness. Because several other island populations of P. lateralis also exhibit exceptionally low levels of genetic variation, this phenomenon may be widespread. Inbreeding in these populations is at a level associated with high rates of extinction in populations of domestic and laboratory species. Genetic factors cannot then be excluded as contributing to the extinction proneness of small, isolated populations.     

Temporal Analysis of Genetic Structure to Assess Population Dynamics of Reintroduced Swift Foxes

Reintroductions are increasingly used to reestablish species, but a paucity of long‐term postrelease monitoring has limited understanding of whether and when viable populations subsequently persist. We conducted temporal genetic analyses of reintroduced populations of swift foxes (Vulpes velox) in Canada (Alberta and Saskatchewan) and the United States (Montana). We used samples collected 4 years apart, 17 years from the initiation of the reintroduction, and 3 years after the conclusion of releases. To assess program success, we genotyped 304 hair samples, subsampled from the known range in 2000 and 2001, and 2005 and 2006, at 7 microsatellite loci. We compared diversity, effective population size, and genetic connectivity over time in each population. Diversity remained stable over time and there was evidence of increasing effective population size. We determined population structure in both periods after correcting for differences in sample sizes. The geographic distribution of these populations roughly corresponded with the original release locations, which suggests the release sites had residual effects on the population structure. However, given that both reintroduction sites had similar source populations, habitat fragmentation, due to cropland, may be associated with the population structure we found. Although our results indicate growing, stable populations, future connectivity analyses are warranted to ensure both populations are not subject to negative small‐population effects. Our results demonstrate the importance of multiple sampling years to fully capture population dynamics of reintroduced populations. Análisis Temporal de la Estructura Genética para Evaluar la Dinámica Poblacional de Zorros (Vulpes velox) Reintroducidos     

Comparative Population Genetic Structure of the Rare Woodland Shrub Daviesia suaveolens and Its Common Congener D. mimosoides

Genetic (allozyme) variation and population genetic structure of the rare shrub Daviesia suaveolens , found in only a few large populations on the eastern escarpment of the southern tablelands of New South Wales, were compared to those of its abundant and widespread relative D. mimosoides at both spatially equivalent and rangewide scales. We hypothesized that the rare species is genetically depauperate relative to the common one. We also generated baseline data on D. suaveolens to provide management recommendations for its conservation. Both species had high variation relative to other widespread woody angiosperms. Rangewide, the rare species exhibited lower species-level genetic variation than its common relative but a similar level of variation to that found in D. mimosoides over an equivalent spatial scale. Population-level genetic variation was similar for the two species. Over its small geographic range, D. suaveolens populations were three times as genetically differentiated as D. mimosoides over the same scale, showing a clear northsouth genetic disjunction and as much interpopulation divergence as the common species exhibited rangewide. These results confirm that not all types of rarity have the same genetic implications. Conservation strategies for D. suaveolens need not be concerned about low population-level variation unless populations become significantly smaller than is currently typical. Of more importance is to maintain the high interpopulation differentiation by conserving populations from both the north and south of the species' range.     

Genetic Bottlenecks Driven by Population Disconnection

Abstract: Connectivity among populations plays a crucial role in maintaining genetic variation at a local scale, especially in small populations affected strongly by genetic drift. The negative consequences of population disconnection on allelic richness and gene diversity (heterozygosity) are well recognized and empirically established. It is not well recognized, however, that a sudden drop in local effective population size induced by such disconnection produces a temporary disequilibrium in allelic frequency distributions that is akin to the genetic signature of a demographic bottleneck. To document this effect, we used individual‐based simulations and empirical data on allelic richness and gene diversity in six pairs of isolated versus well‐connected (core) populations of European tree frogs. In our simulations, population disconnection depressed allelic richness more than heterozygosity and thus resulted in a temporary excess in gene diversity relative to mutation drift equilibrium (i.e., signature of a genetic bottleneck). We observed a similar excess in gene diversity in isolated populations of tree frogs. Our results show that population disconnection can create a genetic bottleneck in the absence of demographic collapse.     

Importance of Assessing Population Genetic Structure before Eradication of Invasive Species: Examples from Insular Norway Rat Populations

Abstract:  Determining the inter-island migration abilities of pest species and delimiting eradication units enable more viable long-term eradication campaigns because recurrent colonization from neighboring islands is avoided. We examined the genetic structure of the invasive Norway rat ( Rattus norvegicus ) to identify gene flow between islands and delimit population units at different geographical scales. We investigated variation in eight microsatellite loci in rat populations from 18 islands, representing five archipelagos off the Brittany coast (France). Although most of the islands are isolated from each other, short genetic distances, weak F_ST values between close islands, and a high level of cross-assignment showed that individuals collected on different islands could represent a single population unit. A Bayesian clustering method also supported the existence of high levels of gene flow between some neighboring islands. Thus, the statement "one island equals one population" can be false when inter-island distances are less than a few hundred meters. Genetic studies enable the definition of island clusters among which migration may occur that should be considered eradication units. To avoid reinvasion and to minimize ecological and economic costs, rats on all islands in an eradication unit should be eradicated simultaneously. We suggest that the genetic monitoring we performed here can be applied for management of any pest.