Extinction Risk Of Small Populations Research Articles

Consistent scaling of inbreeding depression in space and time in a house sparrow metapopulation

Inbreeding may increase the extinction risk of small populations. Yet, studies using modern genomic tools to investigate inbreeding depression in nature have been limited to single populations, and little is known about the dynamics of inbreeding depression in subdivided populations over time. Natural populations often experience different environmental conditions and differ in demographic history and genetic composition, characteristics that can affect the severity of inbreeding depression. We utilized extensive long-term data on more than 3,100 individuals from eight islands in an insular house sparrow metapopulation to examine the generality of inbreeding effects. Using genomic estimates of realized inbreeding, we discovered that inbred individuals had lower survival probabilities and produced fewer recruiting offspring than noninbred individuals. Inbreeding depression, measured as the decline in fitness-related traits per unit inbreeding, did not vary appreciably among populations or with time. As a consequence, populations with more resident inbreeding (due to their demographic history) paid a higher total fitness cost, evidenced by a larger variance in fitness explained by inbreeding within these populations. Our results are in contrast to the idea that effects of inbreeding generally depend on ecological factors and genetic differences among populations, and expand the understanding of inbreeding depression in natural subdivided populations.

Artificial barriers prevent genetic recovery of small isolated populations of a low-mobility freshwater fish

Habitat loss and fragmentation often result in small, isolated populations vulnerable to environmental disturbance and loss of genetic diversity. Low genetic diversity can increase extinction risk of small populations by elevating inbreeding and inbreeding depression, and reducing adaptive potential. Due to their linear nature and extensive use by humans, freshwater ecosystems are especially vulnerable to habitat loss and fragmentation. Although the effects of fragmentation on genetic structure have been extensively studied in migratory fishes, they are less understood in low-mobility species. We estimated impacts of instream barriers on genetic structure and diversity of the low-mobility river blackfish (Gadopsis marmoratus) within five streams separated by weirs or dams constructed 45–120 years ago. We found evidence of small-scale (<13 km) genetic structure within reaches unimpeded by barriers, as expected for a fish with low mobility. Genetic diversity was lower above barriers in small streams only, regardless of barrier age. In particular, one isolated population showed evidence of a recent bottleneck and inbreeding. Differentiation above and below the barrier (FST = 0.13) was greatest in this stream, but in other streams did not differ from background levels. Spatially explicit simulations suggest that short-term barrier effects would not be detected with our data set unless effective population sizes were very small (<100). Our study highlights that, in structured populations, the ability to detect short-term genetic effects from barriers is reduced and requires more genetic markers compared to panmictic populations. We also demonstrate the importance of accounting for natural population genetic structure in fragmentation studies.

Survival and divergence in a small group: The extraordinary genomic history of the endangered Apennine brown bear stragglers

About 100 km east of Rome, in the central Apennine Mountains, a critically endangered population of ∼50 brown bears live in complete isolation. Mating outside this population is prevented by several 100 km of bear-free territories. We exploited this natural experiment to better understand the gene and genomic consequences of surviving at extremely small population size. We found that brown bear populations in Europe lost connectivity since Neolithic times, when farming communities expanded and forest burning was used for land clearance. In central Italy, this resulted in a 40-fold population decline. The overall genomic impact of this decline included the complete loss of variation in the mitochondrial genome and along long stretches of the nuclear genome. Several private and deleterious amino acid changes were fixed by random drift; predicted effects include energy deficit, muscle weakness, anomalies in cranial and skeletal development, and reduced aggressiveness. Despite this extreme loss of diversity, Apennine bear genomes show nonrandom peaks of high variation, possibly maintained by balancing selection, at genomic regions significantly enriched for genes associated with immune and olfactory systems. Challenging the paradigm of increased extinction risk in small populations, we suggest that random fixation of deleterious alleles (i) can be an important driver of divergence in isolation, (ii) can be tolerated when balancing selection prevents random loss of variation at important genes, and (iii) is followed by or results directly in favorable behavioral changes.

Using demographic characteristics of populations to detect spatial fragmentation following suspected ebola outbreaks in great apes.

Demographic crashes due to emerging diseases can contribute to population fragmentation and increase extinction risk of small populations. Ebola outbreaks in 2002-2004 are suspected to have caused a decline of more than 80% in some Western lowland gorilla (Gorilla gorilla gorilla) populations. We investigated whether demographic indicators of this event allowed for the detection of spatial fragmentation in gorilla populations. We collected demographic data from two neighbouring populations: the Lokoué population, suspected to have been affected by an Ebola outbreak (followed from 2001 to 2014), and the Romani population, of unknown demographic status before Ebola outbreaks (followed from 2005 to 2014). Ten years after the outbreak, the Lokoué population is slowly recovering and the short-term demographic indicators of a population crash were no longer detectable. The Lokoué population has not experienced any additional demographic perturbation over the past decade. The Romani population did not show any of the demographic indicators of a population crash over the past decade. Its demographic structure remained similar to that of unaffected populations. Our results highlighted that the Ebola disease could contribute to fragmentation of gorilla populations due to the spatially heterogeneous impact of its outbreaks. The demographic structure of populations (i.e., age-sex and group structure) can be useful indicators of a possible occurrence of recent Ebola outbreaks in populations without known history, and may be more broadly used in other emerging disease/species systems. Longitudinal data are critical to our understanding of the impact of emerging diseases on wild populations and their conservation.

Floaters may buffer the extinction risk of small populations: an empirical assessment.

The high extinction risk of small populations is commonly explained by reductions in fecundity and breeder survival associated with demographic and environmental stochasticity. However, ecological theory suggests that population extinctions may also arise from reductions in the number of floaters able to replace the lost breeders. This can be particularly plausible under harsh fragmentation scenarios, where species must survive as small populations subjected to severe effects of stochasticity. Using a woodpecker study in fragmented habitats (2004-2016), we provide here empirical support for the largely neglected hypothesis that floaters buffer population extirpation risks. After controlling for population size, patch size and the intrinsic quality of habitat, populations in patches with floaters had a lower extinction probability than populations in patches without floaters (0.013 versus 0.131). Floaters, which often replace the lost breeders, were less likely to occur in small and low-quality patches, showing that population extirpations may arise from unnoticed reductions in floater numbers in poor-quality habitats. We argue that adequate pools of the typically overlooked floaters may buffer extirpation risks by reducing the detrimental impacts of demographic and environmental stochasticity. However, unravelling the influence of floaters in buffering stochastic effects and promoting population stability require additional studies in an ample array of species and stochastic scenarios.

(Re)appreciating the role of life history in eco‐evolutionary dynamics

(Re)appreciating the role of life history in eco‐evolutionary dynamics

Genetic Allee effects and their interaction with ecological Allee effects.

It is now widely accepted that genetic processes such as inbreeding depression and loss of genetic variation can increase the extinction risk of small populations. However, it is generally unclear whether extinction risk from genetic causes gradually increases with decreasing population size or whether there is a sharp transition around a specific threshold population size. In the ecological literature, such threshold phenomena are called 'strong Allee effects' and they can arise for example from mate limitation in small populations. In this study, we aim to (i) develop a meaningful notion of a 'strong genetic Allee effect', (ii) explore whether and under what conditions such an effect can arise from inbreeding depression due to recessive deleterious mutations, and (iii) quantify the interaction of potential genetic Allee effects with the well-known mate-finding Allee effect. We define a strong genetic Allee effect as a genetic process that causes a population's survival probability to be a sigmoid function of its initial size. The inflection point of this function defines the critical population size. To characterize survival-probability curves, we develop and analyse simple stochastic models for the ecology and genetics of small populations. Our results indicate that inbreeding depression can indeed cause a strong genetic Allee effect, but only if individuals carry sufficiently many deleterious mutations (lethal equivalents). Populations suffering from a genetic Allee effect often first grow, then decline as inbreeding depression sets in and then potentially recover as deleterious mutations are purged. Critical population sizes of ecological and genetic Allee effects appear to be often additive, but even superadditive interactions are possible. Many published estimates for the number of lethal equivalents in birds and mammals fall in the parameter range where strong genetic Allee effects are expected. Unfortunately, extinction risk due to genetic Allee effects can easily be underestimated as populations with genetic problems often grow initially, but then crash later. Also interactions between ecological and genetic Allee effects can be strong and should not be neglected when assessing the viability of endangered or introduced populations.

A preliminary population viability analysis of the critically endangered blue-eyed black lemur (Eulemur flavifrons)

Population viability analysis is an important tool to assess the extinction risk in small populations of highly specialized primates. The blue-eyed black lemur (Eulemur flavifrons) is critically endangered with a restricted range in the north-western dry deciduous forest of Madagascar, where habitat fragmentation and loss of forest connectivity threaten its survival. We performed a population viability analysis (PVA) of this lemur in Ankarafa Forest in the Sahamalaza Peninsula National Park, north-western Madagascar, to determine the demographic parameters most influential for population persistence and to assess extinction probabilities. We conducted PVA analyses using different demographic parameters which characterize the species including reproduction, lifespan and population size using the software VORTEX for six scenarios with 100 iterations and simulated over 100 years. The simulations suggested the first extinction within 13 years when the percentage of habitat destruction increased up to 12%. Severe habitat destruction such as fire and logging was the major cause which led to the risk of population extinction. Conservation strategies, in particular measures to reduce habitat destruction, are proposed to ensure the survival of this critically endangered lemur. Une Analyse de viabilité de population (AVP) est un outil important pour évaluer le risque d'extinction de petites populations de primates très spécialisés. Le lémur aux yeux turquoise (Eulemur flavifrons) est en danger critique d'extinction, avec une aire de répartition qui se limite à une forêt sèche décidue du nord-ouest de Madagascar, où la fragmentation de l'habitat et la perte de connectivité de la forêt menacent sa survie. Nous avons réalisé une AVP de ce lémurien dans la forêt d'Ankarafa, dans le Parc National de la Péninsule de Sahamalaza, au nord-ouest de Madagascar, pour déterminer quels étaient les paramètres démographiques qui avaient le plus d'influence sur le maintien de la population et pour évaluer ses probabilités d'extinction. Nous avons fait des AVP en nous servant de différents paramètres démographiques qui caractérisent cette espèce, comme la reproduction, la durée de vie et la taille de la population, en utilisant le logiciel VORTEX pour six scénarios, avec 100 itérations, simulés sur 100 ans. Les simulations suggéraient la première extinction dans 13 ans, lorsque le pourcentage de destruction de l'habitat passait à 12%. Une grave destruction de l'habitat, par le feu ou les coupes d'arbres, était la cause majeure conduisant au risque d'extinction de la population. Des stratégies de conservation, en particulier des mesures pour réduire la destruction de l'habitat, sont proposées pour assurer la survie de ce lémur en danger critique d'extinction.

Severe Habitat Fragmentation Leads to Declines in Genetic Variation, Mate Availability, and Reproductive Success in Small Populations of a Once-Common Australian Grassland Daisy

Premise of research. Inference concerning the impact of habitat fragmentation on genetic variation and demography of plant species is a key theme in conservation biology. For once-common Australian temperate grassland species where there has been almost complete habitat loss, generalizations about habitat fragmentation are unclear because most prior study has focused on rare species.Methodology. We examine the relationship between population setting (density, isolation), reproductive population size (n = 26 to >8000 flowering plants), and genetic variation by using allozyme markers, field seed set, and laboratory germination and growth in fragmented populations of the grassland daisy Leucochrysum albicans var. tricolor, a species once common across southeastern Australia.Pivotal results. Allelic richness, observed and expected heterozygosity, percent seed set, and seed germination were all positively and significantly correlated with log population size (). There was no significant association, however, between log population size and the level of polymorphism, the inbreeding coefficient, or plant fitness (measured as biomass at 28 wk). Diallel crossing showed that small populations were mate limited, suggesting that erosion of allelic richness at self-incompatibility loci may be responsible for lower and variable reproductive output.Conclusions. The outcomes of habitat fragmentation on plant population persistence of common species are likely mediated by population size, as this impacts mate availability via loss of genetic diversity. This will likely elevate the extinction risk of small populations in the long term in ecosystems where there has been intensive long-term land use and population losses and may require conservation measures that include genetic rescue to recover small populations.

Restricted gene flow and genetic drift in recently fragmented populations of an endangered steppe bird

Identifying the genetic processes derived from habitat fragmentation is critical for the conservation of endangered species. We conducted an integrated analysis of genetic patterns in the endangered Dupont’s lark ( Chersophilus duponti), a circum-Mediterranean songbird threatened by the loss and fragmentation of natural steppes in recent decades. After sampling all the remaining Spanish populations and the two closest North African ones, we found that the Mediterranean Sea acts as a major barrier against gene flow and that recent habitat fragmentation is isolating Spanish populations at different spatial scales. While we found a historical signal of gene flow among Spanish regions, a coalescent model supported that the ancestral panmictic population is evolving into several different units in the absence of current gene flow, genetic drift being more intense in the smaller and more isolated populations. Moreover, small-scale spatial autocorrelation analyses showed that genetic differentiation is also acting within populations. The spatial genetic structure, significant levels of inbreeding and high relatedness within patches raise concerns on the viability of most of the extant populations. We highlight the urgency for steppe patches to be protected, expanded and reconnected, considering the genetic clusters identified here rather than the previously considered eco-geographic regions occupied by the species. Meanwhile, translocations could be considered as a complementary, faster management action to attenuate the crowding and genetic effects of population fragmentation and the extinction risk of small populations without compromising the current local adaptations, culture diversity and genetic clusters already known for the species.

Trapped in the extinction vortex? Strong genetic effects in a declining vertebrate population

BackgroundInbreeding and loss of genetic diversity are expected to increase the extinction risk of small populations, but detailed tests in natural populations are scarce. We combine long-term population and fitness data with those from two types of molecular markers to examine the role of genetic effects in a declining metapopulation of southern dunlins Calidris alpina schinzii, an endangered shorebird.ResultsThe decline is associated with increased pairings between related individuals, including close inbreeding (as revealed by both field observations of parentage and molecular markers). Furthermore, reduced genetic diversity seems to affect individual fitness at several life stages. Higher genetic similarity between mates correlates negatively with the pair's hatching success. Moreover, offspring produced by related parents are more homozygous and suffer from increased mortality during embryonic development and possibly also after hatching.ConclusionsOur results demonstrate strong genetic effects in a rapidly declining population, emphasizing the importance of genetic factors for the persistence of small populations.

Small Populations and Offspring Sex‐Ratio Deviations in Eagles

Stochastic variation of sex ratio has long been appreciated as a potential factor driving small populations to extinction, but it is not the only source of sex-ratio bias in small populations. We examined whether some consequences of sex allocation could affect extinction risk in small populations of size-dimorphic birds such as eagles. We report variations in sex ratio at fledging from a long-term study of a declining population of Spanish Imperial Eagles (Aquila adalberti). Nestling sex-ratio deviation apparently was mediated by age of breeders, whereas territory quality had no obvious effect. Adult-adult pairs produced the same proportion of both sexes in high- or low-density situations, but pairs with at least one member in nonadult plumage class produced more males. As the population declined over a period of years, the proportion of breeders with immature plumage increased; consequently, the proportion of fledgling males increased. However, when population density was high, the proportion of breeders with immature plumage decreased and more female offspring were produced. This relationship between population density, composition of breeder age, and fledgling sex ratios allowed us to make predictions of extinction risk due to nonstochastic deviations of sex ratio in small, declining populations. In the study population, on the basis of the Vortex simulation results, an estimated reduction of 42.5% in predicted mean time to extinction was attributed solely to biased sex ratio.

Relative Contribution of Inbreeding Depression and Eroded Adaptive Diversity to Extinction Risk in Small Populations of Shore Campion

To study the relative importance of inbreeding depression and the loss of adaptive diversity in determining the extinction risk of small populations, we carried out an experiment in which we crossed and self-fertilized founder plants from a single, large population of shore campion (Silene littorea Brot.). We used the seeds these plants produced to colonize 18 new locations within the distribution area of the species. The reintroduced populations were of three kinds: inbred and genetically homogeneous, each made up of selfed seed from a single plant; inbred and mixed, made up of a mixture of selfed seeds from all founder plants; and outbred and mixed, made up of a mixture of seeds obtained in outcrosses between the founders. We compared the inbred homogeneous populations with the inbred mixed to measure the effect of genetic diversity among individuals and the inbred mixed with the outbred mixed to measure the effect of inbreeding. Reintroduction success was seriously limited by inbreeding, whereas it was not affected by genetic diversity. This observation and the nonsignificant interaction between family and reintroduction location for individual plant characters suggest that the fixation of overall deleterious genes causing inbreeding depression posed a more serious threat to the short-term survival of the populations than the loss of genes involved in genotype and environment interactions. Thus, reintroduction success was related to adaptive diversity. Preventing such fixation might be the most important consideration in the genetic management and conservation of shore campion populations.

GENETIC VARIABILITY AND DRIFT LOAD IN POPULATIONS OF AN AQUATIC SNAIL

Population genetic theory predicts that in small populations, random genetic drift will fix and accumulate slightly deleterious mutations, resulting in reduced reproductive output. This genetic load due to random drift (i.e., drift load) can increase the extinction risk of small populations. We studied the relationship between genetic variability (indicator of past population size) and reproductive output in eight isolated, natural populations of the hermaphroditic snail Lymnaea stagnalis. In a common laboratory environment, snails from populations with the lowest genetic variability mature slower and have lower fecundity than snails from genetically more variable populations. This result suggests that past small population size has resulted in increased drift load, as predicted. The relationship between genetic variability and reproductive output is independent of the amount of nonrandom mating within populations. However, reproductive output and the current density of snails in the populations were not correlated. Instead, data from the natural populations suggest that trematode parasites may determine, at least in part, population densities of the snails.

Establishment success and extinction risk in autocorrelated environments

We consider establishment success (and extinction risk of small populations) in fluctuating environments, by means of an inhomogeneous branching process model. In this model it is assumed that individuals reproduce asexually during discrete reproduction periods. Within each period individuals reproduce independently and have random numbers of offspring. Expected numbers of offspring vary over reproduction periods due to random environmental changes. Previous simulation results indicated that there is a positive autocorrelation between the establishment probabilities of invaders in successive reproduction periods when environmental states are independently distributed. This result was never formally proved. In this paper we prove that this is indeed true, regardless of the form of the distribution of environmental states or the offspring distribution (under a monotonicity condition, which holds for biologically realistic models). Furthermore, we prove that it is also true for positively autocorrelated environmental states. We show by a counterexample that in environments with a strong negative autocorrelation establishment probabilities can be negatively autocorrelated. This was further examined through simulations. Our results imply that in independent, positively autocorrelated and weakly negatively autocorrelated environments the probability of success of invasion in different independently varying sites is the highest, followed by sequential invasion. For environments with a strong negative autocorrelation, sequential invasion has the highest probability of success. Effects of autocorrelation were further examined with simulations. From the results it appears that the expected length of ‘runs of bad luck’ is the most crucial factor for establishment success.

DEMOGRAPHIC STOCHASTICITY AND THE VARIANCE REDUCTION EFFECT

Demographic stochasticity is almost universally modeled as sampling variance in a homogeneous population, although it is defined as arising from random variation among individuals. This can lead to serious misestimation of the extinction risk in small populations. Here, we derive analytical expressions showing that the misestimation for each demographic parameter is exactly (in the case of survival) or approximately (in the case of fecundity) proportional to the among-individual variance in that parameter. We also show why this misestimation depends on systematic variation among individuals, rather than random variation. These results indicate that correctly assessing the importance of demographic stochasticity requires (1) an estimate of the variance in each demographic parameter; (2) information on the qualitative shape (convex or concave) of the mean–variance relationship; and (3) information on the mechanisms generating among-individual variation. An important consequence is that almost all population viability analyses (PVAs) overestimate the importance of demographic stochasticity and, therefore, the risk of extinction.

Variation among Individuals and Reduced Demographic Stochasticity.

Population viability analysis ( PVA) is a technique that employs stochastic demographic models to predict extinction risk. All else being equal, higher variance in a demographic rate leads to a greater extinction risk. Demographic stochasticity represents variance due to differences among individuals. Current implementations of PVAs, however, assume that the expected fates of all individuals are identical. For example, demographic stochasticity in survival is modeled as a random draw from a binomial distribution. We developed a simple conceptual model showing that if there is variation among individuals in expected survival, then existing PVA models overestimate the variance due to demographic stochasticity in survival. This is a consequence of Jensen's inequality and the fact that the binomial demographic variance is a concave function of mean survival. The effect of variation among individuals on demographic stochasticity in fecundity depends on the mean-variance relationship for individual reproductive success, which is not presently known. If fecundity patterns mirror those of survival, then variation among individuals will reduce the extinction risk of small populations.

Risks of decline and extinction of the endangered Amsterdam albatross and the projected impact of long-line fisheries

The Amsterdam albatross ( Diomedea amsterdamensis) is one of the rarest bird species of world avifauna, consisting of a single population in the upland plateau of Amsterdam Island (SE Indian Ocean). All breeding birds of the population are today banded and a monitoring program involving mark-recapture procedures has been carried out continuously over the past 16 years. We present the first estimate of risk of decline for the Amsterdam albatross using a stochastic matrix population model, and evaluate the extent to which the measurement errors in demographic estimates may affect the baseline conservation assessment. We also estimate the potential effect that resumption of long-line fisheries in the vicinity of Amsterdam Island (one the alleged causes for its low numbers in the recent past) may have on the persistence of this population. Our results indicate that, in the absence of any impact of long-line fisheries, the Amsterdam albatross is unlikely to experience a decline larger than 20% of the current population abundance over the next 50 years. Our results point out the difficulty to assess with certainty the extinction risk of small populations despite the availability of long term data on their demography. They suggest that a very cautious approach should be taken for the preservation of small populations of long-lived species that cannot sustain any level of incidental by-catch. Any new long-line fishery resuming in the foraging range of the Amsterdam albatross, but especially close to Amsterdam Island, may rapidly put this species at risk of extinction.

Compensating for our load of mutations: freezing the meltdown of small populations.

We have investigated the reduction of fitness caused by the fixation of new deleterious mutations in small populations within the framework of Fisher's geometrical model of adaptation. In Fisher's model, a population evolves in an n-dimensional character space with an adaptive optimum at the origin. The model allows us to investigate compensatory mutations, which restore fitness losses incurred by other mutations, in a context-dependent manner. We have conducted a moment analysis of the model, supplemented by the numerical results of computer simulations. The mean reduction of fitness (i.e., expected load) scaled to one is approximately n/(n+2Ne), where Ne is the effective population size. The reciprocal relationship between the load and Ne implies that the fixation of deleterious mutations is unlikely to cause extinction when there is a broad scope for compensatory mutations, except in very small populations. Furthermore, the dependence of load on n implies that pleiotropy plays a large role in determining the extinction risk of small populations. Differences and similarities between our results and those of a previous study on the effects of Ne and n are explored. That the predictions of this model are qualitatively different from studies ignoring compensatory mutations implies that we must be cautious in predicting the evolutionary fate of small populations and that additional data on the nature of mutations is of critical importance.

Does inbreeding affect the extinction risk of small populations?: predictions from Drosophila

Abstract A fundamental assumption underlying the importance of genetic risks within conservation biology is that inbreeding increases the extinction probability of populations. Although inbreeding has been shown to have a detrimental impact on individual fitness, its contribution to extinction is still poorly understood. We have studied the consequences of different levels of prior inbreeding for the persistence of small populations using Drosophila melanogaster as a model organism. To this end, we determined the extinction rate of small vial populations differing in the level of inbreeding under both optimal and stress conditions, i.e. high temperature stress and ethanol stress. We show that inbred populations have a significantly higher short-term probability of extinction than non-inbred populations, even for low levels of inbreeding, and that the extinction probability increases with increasing inbreeding levels. In addition, we observed that the effects of inbreeding become greatly enhanced under stressful environmental conditions. More importantly, our results show that the impact of environmental stress becomes significantly greater for higher inbreeding levels, demonstrating explicitly that inbreeding and environmental stress are not independent but can act synergistically. These effects seem long lasting as the impact of prior inbreeding was still qualitatively the same after the inbred populations had been expanded to appreciable numbers and maintained as such for approximately 50 generations. Our observations have significant consequences for conservation biology.