Genetic variability and drift load in populations of an aquatic snail

Abstract 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.     

Population size is weakly related to quantitative genetic variation and trait differentiation in a stream fish

How population size influences quantitative genetic variation and differentiation among natural, fragmented populations remains unresolved. Small, isolated populations might occupy poor quality habitats and lose genetic variation more rapidly due to genetic drift than large populations. Genetic drift might furthermore overcome selection as population size decreases. Collectively, this might result in directional changes in additive genetic variation (V_A) and trait differentiation (Q_ST) from small to large population size. Alternatively, small populations might exhibit larger variation in V_A and Q_ST if habitat fragmentation increases variability in habitat types. We explored these alternatives by investigating V_A and Q_ST using nine fragmented populations of brook trout varying 50‐fold in census size N (179–8416) and 10‐fold in effective number of breeders, N_b (18–135). Across 15 traits, no evidence was found for consistent differences in V_A and Q_ST with population size and almost no evidence for increased variability of V_A or Q_ST estimates at small population size. This suggests that (i) small populations of some species may retain adaptive potential according to commonly adopted quantitative genetic measures and (ii) populations of varying sizes experience a variety of environmental conditions in nature, however extremely large studies are likely required before any firm conclusions can be made.     

Past bottlenecks and current population fragmentation of endangered huemul deer (<Emphasis Type="Italic">Hippocamelus bisulcus</Emphasis>): implications for preservation of genetic diversity

Small populations in fragmented habitats can lose genetic variation through drift and inbreeding. The huemul (Hippocamelus bisulcus) is an endangered deer endemic to the southern Andes of Chile and Argentina. Huemul numbers have declined by 99% and its distribution by 50% since European settlement. The total population is estimated at less than 2,000 individuals and is highly fragmented. At one isolated population in Chilean Patagonia we sampled 56 individuals between 2005 and 2007 and genotyped them at 14 microsatellite loci. Despite low genetic variability (average 2.071 alleles/locus and average H _O of 0.341), a low inbreeding coefficient (F _IS) of 0.009 suggests nearly random mating. Population genetic bottleneck tests suggest both historical and contemporary reductions in population size. Simulations indicated that the population must be maintained at 75% of the current size of 120 individuals to maintain 90% of its current genetic diversity over the next 100 years. Potential management strategies to maintain genetic variability and limit future inbreeding include the conservation and establishment of habitat corridors to facilitate gene flow and the enlargement of protected areas to increase effective population size.     

Phylogeography and population structure of the endangered Tehuantepec jackrabbit <Emphasis Type="Italic">Lepus flavigularis</Emphasis>: implications for conservation

The Tehuantepec jackrabbit (Lepus flavigularis) is an endangered species restricted to a small area in the Isthmus of Tehuantepec, Oaxaca, Mexico. To evaluate its phylogeographic structure, population genetics, and demographic history we sequenced the mitochondrial Control Region hypervariable domain (CR-1) for 42 individuals representing the entire species range. Phylogenetic patterns indicated that this species is subdivided into two highly divergent clades, with an average nucleotide genetic distance of 3.7% (TrN) between them. Clades A and B are geographically distributed in non-overlapping areas to the west and to the east of the Isthmus of Tehuantepec, respectively. Genetic diversity indices showed reduced genetic variability in L. flavigularis when compared to other species of Lepus within main clades and within populations. This low genetic diversity coupled with the restricted distribution to very small areas of occurrence and limited gene flow suggest that genetic drift has played an important role in the evolution of this species. Historical demographic analysis also pointed out that these two clades underwent a recent population expansion that started about 9,000 years ago for clade A and 3,200 years ago for clade B during the Holocene. Consequently, from the conservation perspective our results suggest that populations included in clades A and B should be regarded as distinct evolutionary lineages.     

Genetic variation relevant for the conservation of the narrow endemic Senecio carbonensis (Asteraceae) from the southern Andes

We studied morphological variation, reproductive biology and genetic structure of Senecio carbonensis, a narrow endemic from high elevations of the southern Andes, and compared it to Senecio peteroanus, a closely related widespread congeneric species. Using ANOVAs and discriminant analysis we showed that populations of S. carbonensis were more similar to each other in their morphology, had comparatively limited reproductive capacity and presented lower plant density and more reduced plant cover than populations of S. peteroanus. Similar high genetic variation was found at the population and species level in both species, based on isozyme variation at 14 and 11 putative gene loci that were resolved in S. carbonensis and S. peteroanus, respectively. The two species were genetically distinct. However, the small genetic distance between populations of each species suggests that either they were recently founded and that genetic drift did not have time to promote divergence, or that its effects are masked by significant current gene flow. These results show that ecological and reproductive characteristics of S. carbonensis may limit its extension and abundance. In contrast, high genetic variation at the population level is probably favored by self‐incompatibility. Despite the restricted geographical distribution and low plant density of S. carbonensis populations, genetic characteristics do not seem to be limiting their long‐term persistence. This information suggests that populations of S. carbonensis are not at risk of extinction as a result of genetic factors, although it is important to study and monitor population dynamics to further assess the degree of recruitment through time.     

Low genetic diversity in small peripheral populations of a rare European tree <Emphasis Type="Italic">(Sorbus torminalis)</Emphasis> dominated by clonal reproduction

Analysis of nuclear microsatellites in six small populations of Sorbus torminalis on its northern distribution limit was carried out to evaluate the dominating mode of reproduction as well as genetic diversity within and among populations. Within populations there was a low genetic diversity with heterozygote excess in five populations. Genetic differentiation was high among populations and the amount of clonally arisen recruits was 94–100%. This suggests that clonal growth, small population size and a possible self-incompability system maintain heterozygosity, although some genetic drift would also be expected. The results are discussed with respect to potential conservation strategies for S. torminalis in the study region.     

The Influence of Translocation Strategy and Management Practices on the Genetic Variability of a Reestablished Elk (Cervus elaphus) Population

Reintroduction of terrestrial vertebrates with the goal of ecosystem restoration typically establishes small and isolated populations that may experience reduced genetic variability due to founder effects and genetic drift. Understanding the genetic structure of these populations and maintaining adequate genetic diversity is important for long‐term restoration success. We quantified genetic variability at six microsatellite loci for a reintroduced population of Cervus elaphus (elk) restored to the tallgrass prairie ecosystem of northeastern Kansas. Allelic richness, observed and expected heterozygosity were intermediate to levels reported in other North American elk populations. Current levels of genetic variability in restored North American elk populations were not well explained by founding population size, number of founding populations, or number of years since the last translocation. Simulation results suggest that the retention of genetic variability in isolated populations is strongly influenced by mating system while also being impacted by temporal variability in population size and population growth rate. Our results have implications for understanding how translocation strategies and post‐reintroduction management may influence genetic variability in restored populations.     

Differential phenotypic variability among the Apalachee mission populations of La Florida: a diachronic perspective

Phenotypic variability is evaluated in a series of skeletal samples from the Apalachee region of Florida. Based on ethnohistoric evidence, several predictive models for changes in variability are generated. If variability decreases through time, this likely represents the effect of genetic drift in populations experiencing epidemic disease and population loss. If variability increases through time, this suggests that population aggregation or genetic admixture were primary factors shaping the Apalachee population during the mission period. Dental dimensions were collected from a series of precontact (pre-1500), early mission (AD 1633-1650) (San Pedro y San Pablo de Patale), and late mission (post-1657) (San Luis) samples from the Apalachee region and were subjected to univariate and multivariate variability analyses. The results indicate that the late mission San Luis sample was significantly more variable than the Patale or precontact samples; however, the Patale sample exhibited no significant variability change in comparison to the precontact population. This suggests that the missions initially effected limited change in genetic variability in the mission populations. However, San Luis was affected by either admixture or population aggregation to such a degree that the observed variation had increased beyond earlier levels. Given the limited historic evidence for population aggregation at this mission, and the comparatively large resident Spanish population, the increased variability may be indicative of admixture at this mission, and potentially at this mission only. Based on a limited data set, however, it appears that the mission period cannot be typified by a single evolutionary or historic process.     

Stochastic modelling of shifts in allele frequencies reveals a strongly polygynous mating system in the re‐introduced Asiatic wild ass

Small populations are prone to loss of genetic variation and hence to a reduction in their evolutionary potential. Therefore, studying the mating system of small populations and its potential effects on genetic drift and genetic diversity is of high importance for their viability assessments. The traditional method for studying genetic mating systems is paternity analysis. Yet, as small populations are often rare and elusive, the genetic data required for paternity analysis are frequently unavailable. The endangered Asiatic wild ass (Equus hemionus), like all equids, displays a behaviourally polygynous mating system; however, the level of polygyny has never been measured genetically in wild equids. Combining noninvasive genetic data with stochastic modelling of shifts in allele frequencies, we developed an alternative approach to paternity analysis for studying the genetic mating system of the re‐introduced Asiatic wild ass in the Negev Desert, Israel. We compared the shifts in allele frequencies (as a measure of genetic drift) that have occurred in the wild ass population since re‐introduction onset to simulated scenarios under different proportions of mating males. We revealed a strongly polygynous mating system in which less than 25% of all males participate in the mating process each generation. This strongly polygynous mating system and its potential effect on the re‐introduced population's genetic diversity could have significant consequences for the long‐term persistence of the population in the Negev. The stochastic modelling approach and the use of allele‐frequency shifts can be further applied to systems that are affected by genetic drift and for which genetic data are limited.     

Genetic structuring in fluctuating populations

The effect of genetic drift in spatially distributed dispersal-linked and density-regulated populations is studied in a classical one-locus two-allele system. We analyse emergence of genetic differentiation assuming random drift only, where the noise-like variability is due to demographic stochasticity. We find emergence of clusters of sub-units with local allele fixation and persistence of both alleles in lengthy simulations. We demonstrate that local allele fixation (extending over a number of adjoining spatial sub-units) – without global loss of alleles – may occur when the carrying capacities of local patches are small, under a full range population dynamic regimes, when dispersal rate is small, and when redistribution (through dispersal) does not act as global mixer. These results are novel. The key to the observations is that drift is simultaneously influenced by distance-dependent dispersal, demographic stochasticity and autocorrelated population fluctuations due to delayed-density dependence. These are standard elements of contemporary population models in spatially structured context. With stable large populations, no stochasticity and dispersal limited to neighbours only, our model collapses to the stepping-stone model, while with dispersal being random and global, the model collapses to Wright's island model.     

Differentiation with drift: a spatio-temporal genetic analysis of Galápagos mockingbird populations (Mimus spp.)

Small and isolated island populations provide ideal systems to study the effects of limited population size, genetic drift and gene flow on genetic diversity. We assessed genetic diversity within and differentiation among 19 mockingbird populations on 15 Galápagos islands, covering all four endemic species, using 16 microsatellite loci. We tested for signs of drift and gene flow, and used historic specimens to assess genetic change over the last century and to estimate effective population sizes. Within-population genetic diversity and effective population sizes varied substantially among island populations and correlated strongly with island size, suggesting that island size serves as a good predictor for effective population size. Genetic differentiation among populations was pronounced and increased with geographical distance. A century of genetic drift did not change genetic diversity on an archipelago-wide scale, but genetic drift led to loss of genetic diversity in small populations, especially in one of the two remaining populations of the endangered Floreana mockingbird. Unlike in other Galápagos bird species such as the Darwin''s finches, gene flow among mockingbird populations was low. The clear pattern of genetically distinct populations reflects the effects of genetic drift and suggests that Galápagos mockingbirds are evolving in relative isolation.     

THE INFLUENCE OF SELF-FERTILIZATION AND POPULATION DYNAMICS ON THE GENETIC STRUCTURE OF SUBDIVIDED POPULATIONS: A CASE STUDY USING MICROSATELLITE MARKERS IN THE FRESHWATER SNAIL BULINUS TRUNCATUS

The distribution of neutral genetic variability within and among sets of populations results from the combined actions of genetic drift, migration, extinction and recolonization processes, mutation, and the mating system. We here analyzed these factors in 38 populations of the hermaphroditic snail Bulinus truncatus. The sampling area covered a large part of the species range. The variability was analyzed using four polymorphic microsatellite loci. A very large number of alleles (up to 55) was found at the level of the whole study. Observed heterozygote deficiencies within populations are consistent with very high selfing rates, generally above 0.80, in all populations. These should depress the variability within populations, because of low effective size, genetic hitchhiking, and background selection, whatever the model of mutation assumed. However, that some populations exhibit much more variability than others suggests that historical demographic processes (e.g., population size variation, bottlenecks, or founding events) may play a significant role. A hierarchical analysis of the distribution of the variability across populations indicates a strong pattern of isolation by distance, whatever the geographical scale considered. Our analysis also illustrates how the mutation rate may affect population differentiation, as different mutation rates result in different levels of homoplasy at microsatellite loci. The effects of both genetic drift and gene flow vary with the temporal and spatial scales considered in B. truncatus populations.     

Temporal increase in mtDNA diversity in a declining population

In small and declining populations levels of genetic variability are expected to be reduced due to effects of inbreeding and random genetic drift. As a result, both individual fitness and populations’ adaptability can be compromised, and the probability of extinction increased. Therefore, maintenance of genetic variability is a crucial goal in conservation biology. Here we show that although the level of genetic variability in mtDNA of the endangered Fennoscandian lesser white‐fronted goose Anser erythropus population is currently lower than in the neigbouring populations, it has increased six‐fold during the past 140 years despite the precipitously declining population. The explanation for increased genetic diversity in Fennoscandia appears to be recent spontaneous increase in male immigration rate equalling 0.56 per generation. This inference is supported by data on nuclear microsatellite markers, the latter of which show that the current and the historical Fennoscandian populations are significantly differentiated (F_ST = 0.046, P = 0) due to changes in allele frequencies. The effect of male‐mediated gene flow is potentially dichotomous. On the one hand it may rescue the Fennoscandian lesser white‐fronted goose from loss of genetic variability, but on the other hand, it eradicates the original genetic characteristics of this population.     

Limited genetic diversity of an endemic subspecies Schizopygopsis chengi baoxingensis as inferred from the mitochondrial DNA control region

As a subspecies of Schizopygopsis chengi (Fang), Schizopygopsis chengi baoxingensis (Fu, Ding et Ye) occurs as a single population endemic to the Baoxing River in China. The influences from the construction of hydropower dams in its distribution area might result in its extinction in the future due to its very narrow habitat and small population size. In this study, we sequenced the mitochondrial DNA control region of 81 individuals to analyze the genetic variability of the subspecies, hoping to acquire basic genetic information. The results revealed a limited genetic diversity of the population. Total samples could only be defined as seven haplotypes based on nucleotide variations. The nucleotide diversity (0.0008), haplotype diversity (0.534), and overall mean genetic distance among individuals (0.00080 ± 0.00053) were very low. Therefore, it is very necessary and urgent to conserve the population of this subspecies, avoiding further genetic loss, or even extinction. Handling editor: Christian Sturmbauer     

Molecular changes in the maize composite EPS12 during selection for resistance to pink stem borer

The pink stem borer (Sesamia nonagrioides Lefèvbre) is the most important pest of maize (Zea mays L.) throughout the Mediterranean area. The maize composite EPS12 has been chosen as the base population for a breeding program based on its resistance to pink stem borer, with the main selection criterion being resistance to stem tunneling. Yield was taken as a secondary selection criterion to avoid any unwanted negatively correlated response on this character. The aims of investigation were: (1) to monitor the effects of selection for resistance to pink stem borer on allele frequency at 70 simple sequence repeat (SSR) markers and their impact on the genetic structure of EPS12 and (2) to identify loci at which allelic frequencies changed significantly due to directional selection. Genetic diversity was reduced during the selection process (as expected since random genetic drift as well as selection could reduce genetic variability), but not significantly so. Although the loss of genetic variation was generally consistent with that expected in a model in which random genetic drift acts alone on neutral alleles, the changes observed in the frequency of five alleles were significantly greater than expected. Further, the linear trend of the departure from the random genetic drift model was significant for some allelic versions of two SSR markers, umc1329 and phi076; directional selection was therefore acting on these loci. The significant effect of directional selection on those markers suggests the presence of quantitative trait loci (QTLs) for tunnel length and/or for yield under artificial infestation with Sesamia nonagrioides on the long arm of chromosome 4.     

Local adaptation through genetic differentiation in highly fragmented Tilia cordata populations

We assessed the level of geographic differentiation of Tilia cordata in Denmark based on tests of 91 trees selected from 12 isolated populations. We used quantitative analysis of spring phenology and population genetic analysis based on SSR markers to infer the likely historical genetic processes within and among populations. High genetic variation within and among populations was observed in spring phenology, which correlated with spring temperatures at the origin of the tested T. cordata trees. The population genetic analysis revealed significant differentiation among the populations, but with no clear sign of isolation by distance. We infer the findings as indications of ongoing fine scale selection in favor of local growth conditions made possible by limited gene flow among the small and fragmented populations. This hypothesis fits well with reports of limited fruiting in the investigated Danish T. cordata populations, while the species is known for its ability to propagate vegetatively by root suckers. Our results suggest that both divergent selection and genetic drift may have played important roles in forming the genetic patterns of T. cordata at its northern distribution limit. However, we also speculate that epigenetic mechanism arising from the original population environment could have created similar patterns in regulating the spring phenology.     

Long-term population genetic structure of an invasive urochordate: the ascidian Botryllus schlosseri

The accelerated pace of marine biological invasions raises questions pertaining to genetic traits and dynamics underlying the successful establishment of invasive species. Current research stresses the importance of multiple introductions and prolonged gene flow as the main sources for genetic diversity, which, along with genetic drift, affect invasive species success. We here attempt to determine the relative contribution of gene flow and mutation rates as sources of genetic variability using the invasive tunicate Botryllus schlosseri as a model. The study was performed over a 13-year period in the Santa Cruz Harbor, California. With a characteristic life history of five generations/year, the Santa Cruz Botryllus population has already experienced approximately 155 generations since the onset of its invasion. The results (278 specimens, 127 scored alleles, five microsatellite loci) support limited gene flow rate (2.89?×?10^?3) and relative genetic isolation. Furthermore, the study population was found to be influenced by both, genetic drift and a high mutation rate (2.47?×?10^?2). These findings were supported by high fluctuations in the frequencies of microsatellite alleles, the appearance of new alleles and the loss of others. The balance between genetic drift and a high mutation rate is further elucidated by the high, stable level of genetic variation. We suggest that rapid mutation rates at the microsatellite loci reflect genome-wide phenomena, helping to maintain high genetic variability in relatively isolated populations. The potential adaptability to new environments is discussed.     

The genetic structure of the loggerhead sea turtle (Caretta caretta) in the Mediterranean as revealed by nuclear and mitochondrial DNA and its conservation implications

The population genetic structure of the loggerhead sea turtle (Caretta caretta) nesting in the eastern Mediterranean was assessed by sequencing a fragment of the control region of the mitochondrial DNA (n = 190) and seven microsatellites (n = 112). The two types of markers revealed genetic structuring (mtDNA: γ_st = 0.212, P < 0.001; nDNA F _st = 0.006, P < 0.001), thus indicating that both females and males are philopatric and that gene flow between populations is restricted. Mitochondrial DNA data indicate that the female populations nesting on the islands of Crete and Cyprus have suffered a recent bottleneck or colonization event. However, no bottleneck or founder effect was revealed by nuclear markers, thus indicating male-mediated gene flow from other populations that would increase nuclear genetic variability. Crete, and to a lower extent Cyprus, are thought to play a central role in such male-mediated gene flow that may reduce the negative effect of genetic drift or inbreeding on the small populations of Lebanon and Israel. This population structure indicates that assessing population relevance only on the basis of genetic variability and size would be misleading, as some populations not fulfilling those requirements may play a relevant role in genetic exchange and hence contribute to the overall genetic variability.     

RAPD variation among and within small and large populations of the rare clonal plant Ranunculus reptans (Ranunculaceae)

In the pre-alpine region of Europe numbers and sizes of populations of the clonal lake shore plant Ranunculus reptans have declined because of the regulation of lake water levels. We investigated genetic variation among and within 17 populations of different size (cover 1–10 000 m²) in R. reptans with RAPD (random amplified polymorphic DNA) profiles. We sampled 127 rosettes in 14 populations at Lake Constance and three populations at or near Lake Como. There was significant genetic variation between plants from the two lake regions (5.9%, analysis of molecular variance [AMOVA], P < 0.001), among populations within lake regions (20.4%, P < 0.001), and within populations (73.7%, P < 0.001). Under the assumptions of Wright's island model the variation among populations corresponds to a gene flow of N_em = 0.70. Within the 14 Lake Constance populations we detected significant genetic variation among subpopulations separated by only a few metres (4.0% of the within-population variation; P < 0.05). Molecular variance was 24% smaller in small populations covering <100 m² area than in larger ones (P < 0.03), indicating that samples from large populations were genetically more variable than samples representing comparable areas of smaller populations. We conclude that gene flow among populations is very limited and that genetic drift has caused reduced genetic variability of smaller populations. Conservation of genetic variability in R. reptans requires persistence of large and also of small populations (because of population differentiation), and it could be enhanced by increasing the size of small populations (to counter genetic drift).     

Niche width and variation within and between populations in colonizing species (Carex flava group)

Summary Taxa of the Carex flava group in Switzerland show a trend towards increased colonizing ability (r-selection). High colonizing ability is correlated with a large fundamental but a small and discontinuous realized niche. It is argued that r-selected species with wide niches should be monomorphic with generalists rather than polymorphic with specialists since they have small effective population sizes in which high genetic variability cannot be maintained. The most r-selected taxon of the group, C. viridula spp. viridula, has indeed the lowest genetic variability within populations but, in ecologically important characters, expresses the highest plasticity. The taxonomically important characters (inflorescences) have high heritability and differences between populations of C. viridula ssp. viridula are probably much affected by genetic drift.