Genetic variation in a semi-natural Drosophila population after a bottleneck I. Lethals,their allelism and effective population size

A semi-natural Drosophila melanogaster population was twice forced through a genetic bottleneck and allowed to recover naturally. In one case additional variation was introduced to the recovering population. The percentage of lethal chromosomes, the level of allelism between these lethals, and the effective population size calculated from the allelism of these lethals all rose sharply in the few generations following each bottleneck, though this was not the case in the very first generation. Thereafter this rise decelerated rapidly and never returned to pre-bottleneck levels. Additional introduced variation had little effect. The reasons for and implications of this pattern have been considered.     

Using heterozygosity–fitness correlations to study inbreeding depression in an isolated population of white‐tailed deer founded by few individuals

A heterozygosity–fitness correlations (HFCs) may reflect inbreeding depression, but the extent to which they do so is debated. HFCs are particularly likely to occur after demographic disturbances such as population bottleneck or admixture. We here study HFC in an introduced and isolated ungulate population of white‐tailed deer Odocoileus virginianus in Finland founded in 1934 by four individuals. A total of 422 ≥ 1‐year‐old white‐tailed deer were collected in the 2012 hunting season in southern Finland and genotyped for 14 microsatellite loci. We find significant identity disequilibrium as estimated by g₂. Heterozygosity was positively associated with size‐ and age‐corrected body mass, but not with jaw size or (in males) antler score. Because of the relatively high identity disequilibrium, heterozygosity of the marker panel explained 51% of variation in inbreeding. Inbreeding explained approximately 4% of the variation in body mass and is thus a minor, although significant source of variation in body mass in this population. The study of HFC is attractive for game‐ and conservation‐oriented wildlife management because it presents an affordable and readily used approach for genetic monitoring that allowing identification of fitness costs associated with genetic substructuring in what may seem like a homogeneous population.     

Purging of inbreeding depression and fitness decline in bottlenecked populations of Drosophila melanogaster

Drastic reductions in population size, or bottlenecks, are thought to significantly erode genetic variability and reduce fitness. However, it has been suggested that a population can be purged of the genetic load responsible for reduced fitness when subjected to bottlenecks. To investigate this phenomenon, we put a number of Drosophila melanogaster isofemale lines known to differ in inbreeding depression through four ‘founder‐flush’ bottleneck cycles with flush sizes of 5 or 100 pairs and assayed for relative fitness (single‐pair productivity) after each cycle. Following the founder‐flush phase, the isofemale lines, with a large flush size and a history of inbreeding depression, recovered most of the fitness lost from early inbreeding, consistent with purging. The same isofemale lines, with a small flush size, did not regain fitness, consistent with the greater effect of genetic drift in these isofemale lines. On the other hand, the isofemale lines that did not show initial inbreeding depression declined in fitness after repeated bottlenecks, independent of the flush size. These results suggest that the nature of genetic variation in fitness may greatly influence the way in which populations respond to bottlenecks and that stochastic processes play an important role. Consequently, an attempt intentionally to purge a population of detrimental variation through inbreeding appears to be a risky strategy, particularly in the genetic management of endangered species.     

Variability of Wing Size and Shape in Three Populations of a Recent Brazilian Invader, Zaprionus indianus (Diptera: Drosophilidae), from Different Habitats

Zaprionus indianus (Diptera: Drosophilidae) is an African species that was introduced in Brazil near the end of the 1990’s decade. To evaluate the adaptive potential of morphological traits in natural populations of this recently introduced species, we have investigated wing size and shape variation at Rio de Janeiro populations only two years after the first record of Z. indianus in Brazil. Significant genetic differences among populations from three distinct ecological habitats were detected. The heritability and evolvability estimates show that, even with the population bottleneck that should have occurred during the invasion event, an appreciable amount of additive genetic variation for wing size and shape was retained. Our results also indicated a greater influence of environmental variation on wing size than on wing shape. The importance of quantitative genetic variability and plasticity in the successful establishment and dispersal of Z. indianus in the Brazilian territory is then discussed.     

Redistribution of gene frequency and changes of genetic variation following a bottleneck in population size

Although the distribution of frequencies of genes influencing quantitative traits is important to our understanding of their genetic basis and their evolution, direct information from laboratory experiments is very limited. In theory, different models of selection and mutation generate different predictions of frequency distributions. When a large population at mutation-selection balance passes through a rapid bottleneck in size, the frequency distribution of genes is dramatically altered, causing changes in observable quantities such as the mean and variance of quantitative traits. We investigate the gene frequency distribution of a population at mutation-selection balance under a joint-effect model of real stabilizing and pleiotropic selection and its redistribution and thus changes of the genetic properties of metric and fitness traits after the population passes a rapid bottleneck and expands in size. If all genes that affect the trait are neutral with respect to fitness, the additive genetic variance (VA) is always reduced by a bottleneck in population size, regardless of their degree of dominance. For genes that have been under selection, VA increases following a bottleneck if they are (partially) recessive, while the dominance variance increases substantially for any degree of dominance. With typical estimates of mutation parameters, the joint-effect model can explain data from laboratory experiments on the effect of bottlenecking on fitness and morphological traits, providing further support for it as a plausible mechanism for maintenance of quantitative genetic variation.     

Investigating the genetic load of an emblematic invasive species: the case of the invasive harlequin ladybird Harmonia axyridis

Introduction events can lead to admixture between genetically differentiated populations and bottlenecks in population size. These processes can alter the adaptive potential of invasive species by shaping genetic variation, but more importantly, they can also directly affect mean population fitness either increasing it or decreasing it. Which outcome is observed depends on the structure of the genetic load of the species. The ladybird Harmonia axyridis is a good example of invasive species where introduced populations have gone through admixture and bottleneck events. We used laboratory experiments to manipulate the relatedness among H. axyridis parental individuals to assess the possibility for heterosis or outbreeding depression in F₁ generation offspring for two traits related to fitness (lifetime performance and generation time). We found that inter‐populations crosses had no major impact on the lifetime performance of the offspring produced by individuals from either native or invasive populations. Significant outbreeding depression was observed only for crosses between native populations for generation time. The absence of observed heterosis is indicative of a low occurrence of fixed deleterious mutations within both the native and invasive populations of H. axyridis. The observed deterioration of fitness in native inter‐population crosses most likely results from genetic incompatibilities between native genomic backgrounds. We discuss the implications of these results for the structure of genetic load in H. axyridis in the light of the available information regarding the introduction history of this species.     

Bottlenecks and rescue effects in a fluctuating population of golden-mantled ground squirrels (Spermophilus lateralis)

Mammal species characterized by highly fluctuating populations often maintain genetic diversity in response to frequent demographic bottlenecks, suggesting the ameliorating influence of life history and behavioral factors. Immigration in particular is expected to promote genetic recovery and is hypothesized to be the most likely process maintaining genetic diversity in fluctuating mammal populations. Most demographic bottlenecks have been inferred retrospectively, and direct analysis of a natural population before, during, and after a bottleneck is rare. Using a continuous 10-year dataset detailing the complete demographic and genetic history of a fluctuating population of golden-mantled ground squirrels (Spermophilus lateralis), we analyzed the genetic consequences of a 4-year demographic bottleneck that reduced the population to seven adult squirrels, and we evaluated the potential “rescue effect” of immigration. Analysis of six microsatellite loci revealed that, while a decline in allelic richness was observed during the bottleneck, there was no observed excess of heterozygosity, a characteristic bottleneck signature, and no evidence for heterozygote deficiency during the recovery phase. In addition, we found no evidence for inbreeding depression during or after the bottleneck. By identifying immigrants and analyzing their demographic and genetic contributions, we found that immigration promoted demographic recovery and countered the genetic effects of the bottleneck, especially the loss of allelic richness. Within 3 years both population size and genetic variation had recovered to pre-bottleneck levels, supporting the role of immigration in maintaining genetic variation during bottleneck events in fluctuating populations. Our analyses revealed considerable variation among analytical techniques in their ability to detect genetic bottlenecks, suggesting that caution is warranted when evaluating bottleneck events based on one technique.     

Rapid loss of MHC class II variation in a bottlenecked population is explained by drift and loss of copy number variation

Population bottlenecks may reduce genetic variation and potentially increase the risk of extinction. Here, we present the first study to use historic samples to analyse loss of variation at the major histocompatibility complex (MHC), which plays a central role in vertebrate disease resistance. Balancing selection acts on the MHC and could moderate the loss of variation expected from drift; however, in a Wisconsin population of greater prairie-chickens (Tympanuchus cupido), the number of MHC class II B alleles per individual declined by 44% following a population bottleneck, compared to a loss of only 8% at microsatellites. Simulations indicate that drift likely reduced MHC variation at the population level, as well as within individuals by reducing the number of gene copies per individual or by fixing the same alleles across multiple loci. These multiple effects of genetic drift on MHC variation could have important implications for immunity and fitness.     

Selection maintains MHC diversity through a natural population bottleneck

A perceived consequence of a population bottleneck is the erosion of genetic diversity and concomitant reduction in individual fitness and evolutionary potential. Although reduced genetic variation associated with demographic perturbation has been amply demonstrated for neutral molecular markers, the effective management of genetic resources in natural populations is hindered by a lack of understanding of how adaptive genetic variation will respond to population fluctuations, given these are affected by selection as well as drift. Here, we demonstrate that selection counters drift to maintain polymorphism at a major histocompatibility complex (MHC) locus through a population bottleneck in an inbred island population of water voles. Before and after the bottleneck, MHC allele frequencies were close to balancing selection equilibrium but became skewed by drift when the population size was critically low. MHC heterozygosity generally conformed to Hardy-Weinberg expectations except in one generation during the population recovery where there was a significant excess of heterozygous genotypes, which simulations ascribed to strong differential MHC-dependent survival. Low allelic diversity and highly skewed frequency distributions at microsatellite loci indicated potent genetic drift due to a strong founder affect and/or previous population bottlenecks. This study is a real-time examination of the predictions of fundamental evolutionary theory in low genetic diversity situations. The findings highlight that conservation efforts to maintain the genetic health and evolutionary potential of natural populations should consider the genetic basis for fitness-related traits, and how such adaptive genetic diversity will vary in response to both the demographic fluctuations and the effects of selection.     

Genetic variability in fallow deer, Dama dama L

Twelve blood proteins and enzymes were tested for polymorphism in a herd of fallow deer, Dama dama L., bred for meat production in Western Germany, to investigate the genetic constitution of the population. Although an enzyme polymorphism was detected (Catalase) for the first time in this species, electrophoretic variation is very low in comparison to other large ungulates. Possible explanations for this finding, such as recent inbreeding and a past genetic bottleneck, are given. The relationship between low genetic variation in biochemical marker systems and fitness is discussed.     

Genetic variability in fallow deer, Dama dama L

Summary. Twelve blood proteins and enzymes were tested for polymorphism in a herd of fallow deer, Dama dama L., bred for meat production in Western Germany, to investigate the genetic constitution of the population. Although an enzyme polymorphism was detected (Catalase) for the first time in this species, electrophoretic variation is very low in comparison to other large ungulates. Possible explanations for this finding, such as recent inbreeding and a past genetic bottleneck, are given. The relationship between low genetic variation in biochemical marker systems and fitness is discussed.     

Recolonization after habitat restoration leads to decreased genetic variation in populations of a terrestrial orchid

Colonization is crucial to habitat restoration projects that rely on the spontaneous regeneration of the original vegetation. However, as a previously declining plant species spreads again, the likelihood of founder effects increases through recurrent population founding and associated serial bottlenecks. We related Amplified Fragment Length Polymorphism markers genetic variation and fitness to colonization history for all extant populations of the outcrossing terrestrial orchid Dactylorhiza incarnata in an isolated coastal dune complex. Around 1970, D. incarnata suffered a severe bottleneck yet ultimately persisted and gradually spread throughout the spatially segregated dune slacks, aided by the restoration of an open vegetation. Genetic assignment demonstrated dispersal to vacant sites from few nearby extant populations and very limited inflow from outside the spatially isolated reserve. Results further indicated that recurrent founding from few local sources resulted in the loss of genetic diversity and promoted genetic divergence (F_ST = 0.35) among populations, but did not influence population fitness. The few source populations initially available and the limited inflow of genes from outside the study reserve, as a consequence of habitat degradation and spatial isolation, may have magnified the genetic effects of recurrent population founding.     

Do bottlenecks increase additive genetic variance?

Because of anthropogenic factors many populations have been at least temporarily reduced to a very small population size. Such reductions could potentially decrease genetic variation and increase the probability of extinction. Analysis of molecular markers has shown a decrease in genetic variation but in many cases this has not reduced the ability of the population to recover from the bottleneck. This apparent paradox is resolved by a consideration of how population bottlenecks can affect additive genetic variance, the relevant measure of ability to respond to selective factors. A bottleneck has the potential to increase additive genetic variance in a population. This may result in an increase in fitness, particularly in populations of conservation concern that are small and lack genetic variation. Here we present a meta-analysis of experimental tests of this prediction using models designed to fit data that is strictly additive and data that has non-additive components. This analysis shows that additive genetic variance in a dataset dominated by morphological traits increases, on average, after a bottleneck event when the inbreeding coefficient is less than 0.3, but neither of the theoretical models alone can adequately explain this result. Because of our inability at present to predict the results of a population bottleneck in a specific case and the probability of extinction associated with small population size we caution against using bottlenecks to increase genetic variance, and thus the fitness, of endangered populations.     

Genetic variability and population structure in Cypriot chukar partridges (Alectoris chukar cypriotes) as determined by microsatellite analysis

For the first time, microsatellite loci were used to study the genetic structure in Alectoris chukar cypriotes. Four of the ten tested microsatellite loci were found to be polymorphic in 33 individuals from four regions of Cyprus. The differentiation test between all the pairs of samples gave non-differentiation exact P values in every case (P>0.05). The posterior probability distribution on the number of source populations indicated only one population (P=0.977); also, a high Bayes factor value (130.020) was obtained. Posterior co-assignment probabilities (measures of similarity) for all pairs of individuals ranged from 0.984 to 1. The global F_IS value was not found to be significant. A recent bottleneck of the Cypriot total partridge population is suggested and this is supported by a significant Wilcoxon test (P=0.031) under the Infinite Alleles Model (IAM) and shifted mode in the alleles frequencies distribution. The results suggest that all the individuals studied belong to only one randomly mating (panmictic) population, with low genetic variation and evidence of recent effective population size reduction (genetic bottleneck). A big hunting pressure exists on the island and about 200,000 captive-bred birds are released every year; these individuals are descendant from a small number of eggs collected in a small area of Cyprus in 1986 and this founder effect could explain the existence of a bottleneck and the low genetic variability.     

Evolution of Fitness in Experimental Populations of Vesicular Stomatitis Virus

The evolution of fitness in experimental clonal populations of vesicular stomatitis virus (VSV) has been compared under different genetic (fitness of initial clone) and demographic (population dynamics) regimes. In spite of the high genetic heterogeneity among replicates within experiments, there is a clear effect of population dynamics on the evolution of fitness. Those populations that went through strong periodic bottlenecks showed a decreased fitness in competition experiments with wild type. Conversely, mutant populations that were transferred under the dynamics of continuous population expansions increased their fitness when compared with the same wild type. The magnitude of the observed effect depended on the fitness of the original viral clone. Thus, high fitness clones showed a larger reduction in fitness than low fitness clones under dynamics with included periodic bottleneck. In contrast, the gain in fitness was larger the lower the initial fitness of the viral clone. The quantitative genetic analysis of the trait ``fitness' in the resulting populations shows that genetic variation for the trait is positively correlated with the magnitude of the change in the same trait. The results are interpreted in terms of the operation of MULLER's ratchet and genetic drift as opposed to the appearance of beneficial mutations.     

Impact of a population bottleneck on symmetry and genetic diversity in the northern elephant seal

Abstract The northern elephant seal (NES) suffered a severe population bottleneck towards the end of the nineteenth century. Theoretical expectations for the impact of population bottlenecks include the loss of genetic diversity and a loss of fitness (e.g. through a disruption of developmental stability); however, there are few direct demonstrations in natural populations. Here, we report on the comparison of archive samples collected prior to and following the NES population bottleneck. Measures of genetic diversity show a loss of variation consistent with expectations and suggest a strong disruption in the pattern of allele frequencies following the bottleneck. Measures of bilateral characters show an increase in fluctuating asymmetry.     

Are bottlenecks associated with colonization? Genetic diversity and diapause variation of native and introduced Rhagoletis completa populations

The success of invasive species appears to be a paradox: despite experiencing strong population bottlenecks, invasive species are able to successfully establish in new environments. We studied how the walnut husk fly, Rhagoletis completa, was able to successfully colonize California from the Midwestern United States, by examining genetic diversity and diapause variation of native and introduced fly populations. Climate plays an important role in the successful establishment of introduced insects, because insect diapause is highly dependent upon external climatic conditions. We examined if: (1) fly populations show signs of a population bottleneck, (2) native and introduced flies differ in diapause length when exposed to California and Midwestern climatic conditions, and (3) population genetic diversity is related to variation in diapause length. We assessed if fly diapause conformed more to a model of establishment by local adaptation or to a model of a highly plastic “general-purpose genotype”. Our results indicate that only two populations close to the original introduced location showed signs of a population bottleneck, and native and introduced populations did not differ in genetic diversity. Genetic diversity increased in the northern introduced populations, suggesting that multiple introductions have occurred. Flies emerged about 2 weeks earlier under the Midwestern treatment than the California treatment, and introduced flies emerged about a week earlier than native flies. All flies emerged when walnuts are typically available in California. Although variance in diapause length differed between populations, it did not vary between populations or regions. Furthermore, genetic diversity was not associated with diapause variation. Therefore, multiple introductions and a “general-purpose genotype” appear to have facilitated the fly’s invasion into California.     

Genetic structure of an introduced paper wasp,Polistes chinensis antennalis (Hymenoptera,Vespidae) in New Zealand

Several eusocial wasps are prominent invaders to remote islands. The paper wasp Polistes chinensis antennalis is native to East Asia, was introduced to New Zealand in 1979 and has expanded its distribution there. This provides an excellent opportunity to examine the impacts of an initial bottleneck and subsequent expansion on genetic structure. We analysed and compared the genetic population structures of the native (Japan and South Korea) and invasive New Zealand populations. Although 94% of individuals had shared haplotypes detected across both populations, the remaining 6% had private haplotypes identified in only one of the three countries. The genetic variation at microsatellite loci was lower in New Zealand than in native countries, and the genetic structure in New Zealand was clearly distinct from that in its native range. Higher frequencies of diploid‐male‐ and triploid‐female‐producing colonies were detected in New Zealand than in the native countries, showing the reduction in genetic variation via a genetic bottleneck. At least two independent introductions were suggested, and the putative source regions for New Zealand were assigned as Kanto (central island) and Kyushu (south island) in Japan. Serial founder events following the initial introduction were also indicated. The estimated dispersal distance between mother and daughter in New Zealand was twice that in Japan. Thus, the introduction history of P. chinensis antennalis in New Zealand is probably the result of at least two independent introductions, passing through a bottleneck during introduction, followed by population expansion from the point of introduction.     

Evidence for a recent genetic bottleneck in the endangered Florida Keys silver rice rat (<Emphasis Type="Italic">Oryzomys argentatus</Emphasis>) revealed by microsatellite DNA analyses

Low levels of genetic variation are thought to contribute significantly to the higher extinction rates of endemic island populations compared to their mainland counterparts. We used six microsatellite loci to compare the genetic structure of the endangered silver rice rat (Oryzomys argentatus) population in Saddlebunch Key, Florida to the mainland population of the closely related marsh rice rat (Oryzomys palustris natator) in Everglades National Park. Allelic richness and gene diversity are significantly lower in Saddlebunch Key than in the larger mainland population, and the two populations are significantly differentiated as measured by both F-statistics and Bayesian clustering methods. These findings support the classification of the Keys population as a “distinct vertebrate population” by the U.S. Fish and Wildlife Service. Current gene diversity (H _E) is higher than expected under mutation-drift equilibrium in Saddlebunch Key, indicating a genetic bottleneck. The Keys population also exhibits a mode shift in its allele frequency distribution which suggests a very recent bottleneck has occurred and is consistent with reports of recent population declines. Although habitat loss and exotic species pose a more immediate and serious threat to silver rice rats, the continued loss of genetic variation may contribute to their long-term extinction risk due to inbreeding or by lowering the population’s ability to adapt to future environmental changes. The protection of habitat and the removal of introduced predators and competitors may help increase the population size of silver rice rats and lower their risk of extinction, both from a demographic and a genetic perspective.     

The genetic consequences of a demographic bottleneck in an introduced biological control insect

Population bottlenecks may result in the loss of genetic diversity, with potentially negative consequences for species of interest in conservation biology, including rare species, invasive species and biological control agents. We examined mtDNA sequence data and four variable microsatellite loci (SSRs) in the melaleuca psyllid Boreioglycaspis melaleucae, which was introduced from Australia to Florida as a biological control agent of the invasive plant Melaleuca quinquenervia. We sampled psyllids in the native and introduced ranges as well as individuals stored from the original founding population. There was a clear loss of mtDNA haplotype diversity, as well as a loss of rare microsatellite alleles, in the introduced range. However, there was little genetic differentiation between the home and introduced ranges, and no evidence for a genetic bottleneck based on an analysis of heterozygosity with the microsatellite markers. Overall, the data showed that the demographic bottleneck had a limited effect on the genetics of populations in the new range.