Population Size Bottlenecks Research Articles

Is There a Genetic Paradox of Biological Invasion?

Bottlenecks in population size can reduce fitness and evolutionary potential, yet introduced species often become invasive. This poses a dilemma referred to as the genetic paradox of invasion. Three characteristics must hold true for an introduced population to be considered paradoxical in this sense. First, it must pass through a bottleneck that reduces genetic variation. Second, despite the bottleneck, the introduced population must not succumb to the many problems associated with low genetic variation. Third, it must adapt to the novel environment. Some introduced populations are not paradoxical as they do not combine these conditions. In some cases, an apparent paradox is spurious, as seen in introduced populations with low diversity in neutral markers that maintain high genetic variation in ecologically relevant traits. Even when the genetic paradox is genuine, unique aspects of a species' biology can allow a population to thrive. We propose research directions into remaining paradoxical aspects of invasion genetics.

Polymorphism in the TRP8 gene in Kyrgyz population: Putative association with highland adaptation

The human TRPM8 gene encodes a receptor mediating cold sensitivity, and this points to its putative role in cold adaptation. The structural variability of the TRPM8 gene for five single-nucleotide polymorphisms (SNPs) has been studied in the Kyrgyz population. The SNPs are located in the coding regions of the gene, and three of them are confined to a 20-bp segment in exon 7. The frequencies of minor SNP alleles are as follows: rs13004520 G/C = 0.06; rs28901637 A/T = 0.13; rs11562975 G/C = 0.27; rs7593557 G/A = 0.21; rs11563071 C/G = 0.12. The analyzed sample of Kyrgyz population includes 275 individuals living at different altitudes and under drastically different climatic conditions. The frequency of the minor rs11562975 allele in the highlanders (living above 3200 m ASL and higher) is lower by a factor of 1.5 than in the residents of lower regions (760–3000 m ASL; p < 0.01). This result indicates a selective role of rs11562975 in adapting to cold. A comparison of haplotype frequencies in the Kyrgyz population with Europeans, East Asians, and Africans shows a clear narrowing of genotype variation in Europeans in comparison to all the others. Probably, this phenomenon is related to a decline in the population size (bottleneck effect) during evolution. We consider the exon–intron structure of the TRPM8 gene. The epigenetic markers in the vicinity of the gene have been analyzed. Two strong binding sites for insulator ctcf proteins are present there. They are likely to be associated with chromatin conformation and alternative splicing regulation. A structural–functional characterization of genes for the TRP protein family is provided.

Increased relatedness among the neighboring plants from seedling to adult stages in carnaúba wax palm.

The objective of this study was to assess the spatial genetic structure (SGS) at different life stages (cohorts) in a remnant population (N = 101) of Copernicia prunifera in the semiarid region of northeastern Brazil. Using seven inter-simple sequence repeat molecular markers, we were able to analyze 93 loci with 100% polymorphism. Seedlings had the highest level of genetic diversity (HE = 0.411, HO = 0.599), followed by juveniles (HE = 0.394, HO = 0.579) and adults (HE = 0.267, HO = 0.427). Based on analysis of molecular variance, the majority of genetic variations were observed to occur within the life stages (93.42%) rather than between the life stages (6.58%). We found a recent reduction in the population size (bottleneck) based on the number of loci with heterozygosity excess for the two models used (infinite allele = 92 and stepwise = 91). All the life stages showed significant SGS, with positive and significant kinship values. Sp values were 0.040 for seedlings, 0.093 for juveniles, 0.156 for adults, and 0.053 for the total population. We found an increase in SGS from the seedling to adult stages, indicating that the plants were from related adult progenitors. Data from this study can be used in designing effective management and conservation strategies for the species.

Genetic diversity and genetic structure of an endemic Mexican Dusky Rattlesnake (Crotalus triseriatus) in a highly modified agricultural landscape: implications for conservation.

It is necessary to determine genetic diversity of fragmented populations in highly modified landscapes to understand how populations respond to land-use change. This information will help guide future conservation and management strategies. We conducted a population genetic study on an endemic Mexican Dusky Rattlesnake (Crotalus triseriatus) in a highly modified landscape near the Toluca metropolitan area, in order to provide crucial information for the conservation of this species. There was medium levels of genetic diversity, with a few alleles and genotypes. We identified three genetically differentiated clusters, likely as a result of different habitat cover type. We also found evidence of an ancestral genetic bottleneck and medium values of effective population size. Inbreeding coefficients were low and there was a moderate gene flow. Our results can be used as a basis for future research and C. triseriatus conservation efforts, particularly considering that the Trans-Mexican Volcanic Belt is heavily impacted by destructive land-use practices.

Genetic Variability and Structuring of Arctic Charr (Salvelinus alpinus) Populations in Northern Fennoscandia.

Variation in presumably neutral genetic markers can inform us about evolvability, historical effective population sizes and phylogeographic history of contemporary populations. We studied genetic variability in 15 microsatellite loci in six native landlocked Arctic charr (Salvelinus alpinus) populations in northern Fennoscandia, where this species is considered near threatened. We discovered that all populations were genetically highly (mean F ST ≈ 0.26) differentiated and isolated from each other. Evidence was found for historical, but not for recent population size bottlenecks. Estimates of contemporary effective population size (N e) ranged from seven to 228 and were significantly correlated with those of historical N e but not with lake size. A census size (N C) was estimated to be approximately 300 individuals in a pond (0.14 ha), which exhibited the smallest N e (i.e. N e/N C = 0.02). Genetic variability in this pond and a connected lake is severely reduced, and both genetic and empirical estimates of migration rates indicate a lack of gene flow between them. Hence, albeit currently thriving, some northern Fennoscandian populations appear to be vulnerable to further loss of genetic variability and are likely to have limited capacity to adapt if selection pressures change.

Recent Evolution in Rattus norvegicus Is Shaped by Declining Effective Population Size.

The brown rat, Rattus norvegicus, is both a notorious pest and a frequently used model in biomedical research. By analyzing genome sequences of 12 wild-caught brown rats from their presumed ancestral range in NE China, along with the sequence of a black rat, Rattus rattus, we investigate the selective and demographic forces shaping variation in the genome. We estimate that the recent effective population size (Ne) of this species = , based on silent site diversity. We compare patterns of diversity in these genomes with patterns in multiple genome sequences of the house mouse (Mus musculus castaneus), which has a much larger Ne. This reveals an important role for variation in the strength of genetic drift in mammalian genome evolution. By a Pairwise Sequentially Markovian Coalescent analysis of demographic history, we infer that there has been a recent population size bottleneck in wild rats, which we date to approximately 20,000 years ago. Consistent with this, wild rat populations have experienced an increased flux of mildly deleterious mutations, which segregate at higher frequencies in protein-coding genes and conserved noncoding elements. This leads to negative estimates of the rate of adaptive evolution (α) in proteins and conserved noncoding elements, a result which we discuss in relation to the strongly positive estimates observed in wild house mice. As a consequence of the population bottleneck, wild rats also show a markedly slower decay of linkage disequilibrium with physical distance than wild house mice.

Genetic variation in Aechmea winkleri, a bromeliad from an inland Atlantic rainforest fragment in Southern Brazil

We investigated the genetic diversity and structure of Aechmea winkleri Reitz, an endemic bromeliad found in Southern Brazilian Atlantic rainforest. Seven nuclear microsatellite markers were used to analyze 162 samples from four localities sampled throughout the entire geographic distribution of the species. Results indicate relatively high levels of genetic diversity with an average of allelic richness of 3.57, and observed and expected heterozygosity of 0.559 and 0.608, respectively. The within-inbreeding coefficient was low, ranging from −0.011 to 0.094. All localities significantly deviated from Hardy–Weinberg equilibrium with three of them showing heterozygosites deficiency. Most of the genetic variation (96.64%) was found within localities. No reduction in population size (bottleneck) was detected. Low levels of genetic differentiation among localities were found with pairwise FST comparisons varying from 0.021 to 0.075. Bayesian analyses revealed that A. winkleri is composed by two genetic groups. The number of migrants per generation was high (>1), which maintain localities' cohesion and gene flow. Despite genetic erosion was not detected in the present study, our results revealed that the four localities sampled actually represent one population, the only known so far in nature. Management strategies for A. winkleri conservation should be undertaken as it is an endemic species which occurs in a biome that has gone through major deforestation and fragmentation. This would avoid the increase of inbreeding rates and the loss of genetic diversity.

How Population Growth Affects Linkage Disequilibrium

The "LD curve" relates the linkage disequilibrium (LD) between pairs of nucleotide sites to the distance that separates them along the chromosome. The shape of this curve reflects natural selection, admixture between populations, and the history of population size. This article derives new results about the last of these effects. When a population expands in size, the LD curve grows steeper, and this effect is especially pronounced following a bottleneck in population size. When a population shrinks, the LD curve rises but remains relatively flat. As LD converges toward a new equilibrium, its time path may not be monotonic. Following an episode of growth, for example, it declines to a low value before rising toward the new equilibrium. These changes happen at different rates for different LD statistics. They are especially slow for estimates of [Formula: see text], which therefore allow inferences about ancient population history. For the human population of Europe, these results suggest a history of population growth.

The effect of population bottlenecks on mutation rate evolution in asexual populations

In the absence of recombination, a mutator allele can spread through a population by hitchhiking with beneficial mutations that appear in its genetic background. Theoretical studies over the past decade have shown that the survival and fixation probability of beneficial mutations can be severely reduced by population size bottlenecks. Here, we use computational modelling and evolution experiments with the yeast S.cerevisiae to examine whether population bottlenecks can affect mutator dynamics in adapting asexual populations. In simulation, we show that population bottlenecks can inhibit mutator hitchhiking with beneficial mutations and are most effective at lower beneficial mutation supply rates. We then subjected experimental populations of yeast propagated at the same effective population size to three different bottleneck regimes and observed that the speed of mutator hitchhiking was significantly slower at smaller bottlenecks, consistent with our theoretical expectations. Our results, thus, suggest that bottlenecks can be an important factor in mutation rate evolution and can in certain circumstances act to stabilize or, at least, delay the progressive elevation of mutation rates in asexual populations. Additionally, our findings provide the first experimental support for the theoretically postulated effect of population bottlenecks on beneficial mutations and demonstrate the usefulness of studying mutator frequency dynamics for understanding the underlying dynamics of fitness-affecting mutations.

Phylogeography and trans‐Pacific divergence of the rocky shore gastropod Nucella lima

AbstractAimWe have used phylogeographical and multilocus coalescent population genetic methods to reconstruct the Pleistocene biogeographical history of a broadly distributed north Pacific rocky shore gastropod, Nucella lima.LocationNorthern Pacific rim, from south‐eastern Alaska to Hokkaido Island.MethodsWe gathered DNA sequence data from three loci from N. lima, whose current distribution spans the entire North Pacific rim. We used a combination of population genetic summary statistics (Tajima's D, Fu's FS and ΦST), isolation‐with‐migration divergence models, and extended Bayesian skyline plots to reconstruct the recent biogeographical history of this species.ResultsThe largest values of ΦST across all loci were always between eastern and western samples. Population divergence models indicated no gene flow and mid‐Pleistocene divergence times (&gt; 600 ka) between eastern and western populations. Mitochondrial DNA diversity in the east was low, and coalescent‐based estimates of effective population size were significantly smaller in the east 20,000 years ago, at the end of the last glacial period.Main conclusionsThe results are consistent with a hypothesis in which north Pacific populations were separated into eastern and western refugia by 317 ka with no gene flow since the split. Eastern populations probably underwent a severe bottleneck in population size during the last glacial period. The contrasting demographic histories of eastern and western populations are consistent with the general palaeobiogeographical pattern of greater climate‐related extinction of marine taxa in the eastern Pacific.

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.

Dispersal Capacity and Genetic Structure of Arapaima gigas on Different Geographic Scales Using Microsatellite Markers

Despite the ecological and economic importance of the Arapaima gigas (Cuvier 1817), few data about its dispersal capacity are available. The present study was based on the analysis of microsatellite markers in order to estimate the dispersal capacity of the species on fine, meso, and large geographic scales. For this, 561 specimens obtained from stocks separated by distances of up to 25 km (fine scale), 100 km (meso scale), and 1300–2300 km (large scale) were analyzed. The fine scale analysis indicated a marked genetic similarity between lakes, with low genetic differentiation, and significant differences between only a few pairs of sites. Low to moderate genetic differentiation was observed between pairs of sites on a meso scale (100 km), which could be explained by the distances between sites. By contrast, major genetic differentiation was recorded in the large scale analysis, that is, between stocks separated by distances of over 1300 km, with the analysis indicating that differentiation was not related solely to distance. The genetic structuring analysis indicated the presence of two stocks, one represented by the arapaimas of the Mamirauá Reserve, and the other by those of Santarém and Tucuruí. The dispersal of arapaimas over short distances indicates a process of lateral migration within the várzea floodplains, which may be the principal factor determining the considerable homogeneity observed among the várzea lakes. The populations separated by distances of approximately 100 km were characterized by reduced genetic differentiation, which was associated with the geographic distances between sites. Populations separated by distances of over 1300 km were characterized by a high degree of genetic differentiation, which may be related primarily to historical bottlenecks in population size and the sedentary behavior of the species. Evidence was found of asymmetric gene flow, resulting in increasing genetic variability in the population of the Mamirauá Reserve.

Population Genetic Structure and Evidence of Demographic Expansion of the Ayu (Plecoglossus altivelis) in East Asia

Plecoglossus altivelis (ayu) is an amphidromous fish widely distributed in Northeastern Asia from the East China Sea to the northern Japanese coastal waters, encompassing the Korean Peninsula within its range. The shore lines of northeastern region in Asia have severely fluctuated following glaciations in the Quaternary. In the present study, we investigate the population genetic structure and historical demographic change of P. altivelis at a population level in East Asia. Analysis of molecular variance (AMOVA) based on 244 mitochondrial control region DNA sequences clearly showed that as the sampling scope extended to a larger geographic area, genetic differentiation began to become significant, particularly among Northeastern populations. A series of hierarchical AMOVA could detect the genetic relationship of three closely located islands between Korea and Japan that might have been tightly connected by the regional Tsushima current. Neutrality and mismatch distribution analyses revealed a strong signature of a recent population expansion of P. altivelis in East Asia, estimated at 126 to 391 thousand years ago during the late Pleistocene. Therefore it suggests that the present population of P. altivelis traces back to its approximate demographic change long before the last glacial maximum. This contrasts our a priori expectation that the most recent glacial event might have the most crucial effect on the present day demography of marine organisms through bottleneck and subsequent increase of effective population size in this region.

From nature to the laboratory: the impact of founder effects on adaptation

Most founding events entail a reduction in population size, which in turn leads to genetic drift effects that can deplete alleles. Besides reducing neutral genetic variability, founder effects can in principle shift additive genetic variance for phenotypes that underlie fitness. This could then lead to different rates of adaptation among populations that have undergone a population size bottleneck as well as an environmental change, even when these populations have a common evolutionary history. Thus, theory suggests that there should be an association between observable genetic variability for both neutral markers and phenotypes related to fitness. Here, we test this scenario by monitoring the early evolutionary dynamics of six laboratory foundations derived from founders taken from the same source natural population of Drosophila subobscura. Each foundation was in turn three-fold replicated. During their first few generations, these six foundations showed an abrupt increase in their genetic differentiation, within and between foundations. The eighteen populations that were monitored also differed in their patterns of phenotypic adaptation according to their immediately ancestral founding sample. Differences in early genetic variability and in effective population size were found to predict differences in the rate of adaptation during the first 21 generations of laboratory evolution. We show that evolution in a novel environment is strongly contingent not only on the initial composition of a newly founded population but also on the stochastic changes that occur during the first generations of colonization. Such effects make laboratory populations poor guides to the evolutionary genetic properties of their ancestral wild populations.

Microsatellite loci over a thirty-three year period for a malaria parasite (Plasmodium mexicanum): bottleneck in effective population size and effect on allele frequencies

Changes in population allele frequencies may be driven by several forces, including selection and drift, and are revealed only by sampling over many generations. Such studies, however, are rare for protist parasites. Microsatellite allele frequencies for 4 loci were followed in a population of Plasmodium mexicanum, a malaria parasite of lizards in California USA at 1 site from 1978 to 2010. Rapid turnover of the lizards indicates the parasite was studied for a minimum of 33 transmission cycles and possibly twice that number. Sample sizes ranged from 841 to 956 scored parasite clones per locus. DNA was extracted from frozen dried blood and blood removed from stained blood smears from the earliest years, and a verification study demonstrated DNA from the blood smears provided valid genetic data. Parasite prevalence and effective population size (Ne) dropped after 2000, remaining lower for the next decade. For 2 loci, allele frequencies appeared stable for the first 2 decades of the study, but changed more rapidly after the decline in prevalence. Allele frequencies changed more gradually for the other 2 loci. Genetic drift could account for changes in allele frequencies, especially after the drop in prevalence and Ne, but the force of selection could also have driven the observed patterns.

Did a discrete event 200,000–100,000 years ago produce modern humans?

Scenarios for modern human origins are often predicated on the assumption that modern humans arose 200,000–100,000 years ago in Africa. This assumption implies that something ‘special’ happened at this point in time in Africa, such as the speciation that produced Homo sapiens, a severe bottleneck in human population size, or a combination of the two. The common thread is that after the divergence of the modern human and Neandertal evolutionary lineages ∼400,000 years ago, there was another discrete event near in time to the Middle–Late Pleistocene boundary that produced modern humans. Alternatively, modern human origins could have been a lengthy process that lasted from the divergence of the modern human and Neandertal evolutionary lineages to the expansion of modern humans out of Africa, and nothing out of the ordinary happened 200,000–100,000 years ago in Africa.Three pieces of biological (fossil morphology and DNA sequences) evidence are typically cited in support of discrete event models. First, living human mitochondrial DNA haplotypes coalesce ∼200,000 years ago. Second, fossil specimens that are usually classified as ‘anatomically modern’ seem to appear shortly afterward in the African fossil record. Third, it is argued that these anatomically modern fossils are morphologically quite different from the fossils that preceded them.Here I use theory from population and quantitative genetics to show that lengthy process models are also consistent with current biological evidence. That this class of models is a viable option has implications for how modern human origins is conceptualized.

Population Genetics and the Evolution of Geographic Range Limits in an Annual Plant

Abstract Theoretical models of species' geographic range limits have identified both demographic and evolutionary mechanisms that prevent range expansion. Stable range limits have been paradoxical for evolutionary biologists because they represent locations where populations chronically fail to respond to selection. Distinguishing among the proposed causes of species' range limits requires insight into both current and historical population dynamics. The tools of molecular population genetics provide a window into the stability of range limits, historical demography, and rates of gene flow. Here we evaluate alternative range limit models using a multilocus data set based on DNA sequences and microsatellites along with field demographic data from the annual plant Clarkia xantiana ssp. xantiana. Our data suggest that central and peripheral populations have very large historical and current effective population sizes and that there is little evidence for population size changes or bottlenecks associated with colonization in peripheral populations. Whereas range limit populations appear to have been stable, central populations exhibit a signature of population expansion and have contributed asymmetrically to the genetic diversity of peripheral populations via migration. Overall, our results discount strictly demographic models of range limits and more strongly support evolutionary genetic models of range limits, where adaptation is prevented by a lack of genetic variation or maladaptive gene flow.

Inbreeding Depression Is Purged in the Invasive Insect Harmonia axyridis

Bottlenecks in population size reduce genetic diversity and increase inbreeding, which can lead to inbreeding depression. It is thus puzzling how introduced species, which typically pass through bottlenecks, become such successful invaders. However, under certain theoretical conditions, bottlenecks of intermediate size can actually purge the alleles that cause inbreeding depression. Although this process has been confirmed in model laboratory systems, it has yet to be observed in natural invasive populations. We evaluate whether such purging could facilitate biological invasions by using the world-wide invasion of the ladybird (or ladybug) Harmonia axyridis. We first show that invasive populations endured a bottleneck of intermediate intensity. We then demonstrate that replicate introduced populations experience almost none of the inbreeding depression suffered by native populations. Thus, rather than posing a barrier to invasion as often assumed, bottlenecks, by purging deleterious alleles, can enable the evolution of invaders that maintain high fitness even when inbred.

Genetic diversity and integrity of German wildcat ( Felis silvestris) populations as revealed by microsatellites, allozymes, and mitochondrial DNA sequences

As a consequence of persecution and habitat fragmentation, wildcats ( Felis silvestris silvestris) in Western Europe have experienced a severe reduction in population numbers and sizes. The remaining wildcat populations are considered to be endangered by losses of genetic variability and by hybridisation with free-ranging domestic cats. To investigate genetic diversity within and among wild and domestic cat populations in Germany and to estimate the extent of gene flow between both forms, we analysed a total of 266 individuals. PCR-amplification and sequencing of 322 base pairs of a highly variable part of the mitochondrial control region (HV1) of 244 specimens resulted in 41 haplotypes with 31 polymorphic sites. Additionally, eight microsatellite loci were examined for those 244 cats. Moreover, a total of 46 wildcats and 22 domestic cats could be genotyped for 13 polymorphic out of 31 enzyme loci. Genetic variability in both groups was generally high. Variability in domestic cat populations was higher than in wildcat populations. Almost no differentiation between domestic cat populations could be found (F ST for microsatellites=3%). In contrast, wildcat populations differed significantly from one another (F ST for microsatellites=9.55%) Within the smaller wildcat populations, a reduction of genetic diversity was detectable with regard to the nuclear DNA. Wildcat and domestic cat mitochondrial haplotypes were separated, suggesting a very low level of maternal gene flow between both forms. In microsatellites and to a somewhat lesser extent in allozymes, wildcats and domestic cats showed distinct differentiation, suggesting an only low extent of past hybridisation in certain populations. The microsatellite data set indicated a significantly reduced effective population size (bottleneck) in the recent past for one German wildcat population.

Pseudo-cryptic species Arenicola defodiens and Arenicola marina (Polychaeta: Arenicolidae) in Wadden Sea, North Sea and Skagerrak: Morphological and molecular variation

The polychaete Arenicola defodiens, or black lug, was recently described as a morphologically highly similar species alongside the blow lug Arenicola marina. So far it was only known from the British Isles. A double spawning peak was observed earlier in lugworms of the western Wadden Sea. Here, we test the hypothesis that the two spawning peaks represent the two species in sympatry. This hypothesis is refuted on the basis of both morphological and mitochondrial DNA data; both spawning peaks are attributed to A. marina. In spite of this, we confirm, on the basis of new collections as well as re-examination of museum collections, the presence of A. defodiens in the western Wadden Sea, North Sea and also the Skagerrak; its distribution is restricted to habitats which are either submerged or have short emersion times, have relatively coarse sediments and high and stable salinities. Sympatry is common. The species differ strongly in the mitochondrial DNA fragment examined; the observed 14% uncorrected minimum difference amounts to an estimated 33–63 million years since sequence divergence. The amount of intraspecific molecular variation is larger for A. defodiens than for A. marina. This is evidence to suggest that A. marina may have undergone more recent and/or more severe population size bottlenecks.