Historical Effective Population Size Research Articles

Accurate Non-parametric Estimation of Recent Effective Population Size from Segments of Identity by Descent

Existing methods for estimating historical effective population size from genetic data have been unable to accurately estimate effective population size during the most recent past. We present a non-parametric method for accurately estimating recent effective population size by using inferred long segments of identity by descent (IBD). We found that inferred segments of IBD contain information about effective population size from around 4 generations to around 50 generations ago for SNP array data and to over 200 generations ago for sequence data. In human populations that we examined, the estimates of effective size were approximately one-third of the census size. We estimate the effective population size of European-ancestry individuals in the UK four generations ago to be eight million and the effective population size of Finland four generations ago to be 0.7 million. Our method is implemented in the open-source IBDNe software package.

Genetic analysis of stock structure of blue shark (Prionace glauca) in the north Pacific ocean

The blue shark (Prionace glauca) is globally distributed, occupying the pelagic, open ocean in temperate and tropical waters. It is the most abundant shark in the north Pacific and is exploited in several fisheries. Catch size and sex composition in fisheries and research data, along with tagging and distribution patterns, have been used to infer the existence of distinct north and south Pacific stocks. The present study consisted of a comprehensive survey of nuclear genetic diversity at microsatellite loci within and among six regions encompassing the north Pacific blue shark distribution to rationalize current management practice which assumes a single stock. We tested microsatellite diversity at 14 loci in 786 tissue samples for east–west population differentiation, examined regional samples for evidence of population mixture, and estimated historical and contemporary effective population sizes (Ne). The results strongly supported the existence of a single population of blue shark in the north Pacific. Historical and contemporary Ne values between 4500 and 5500 and the resultant low ratio of effective to census size (Nc) does not reflect recent population perturbation. However, it does highlight that the population may be more vulnerable to reduced reproductive success arising from natural or fishing mortality coupled with environmental change than total abundance would imply.

Temporal Dynamics of Avian Populations during Pleistocene Revealed by Whole-Genome Sequences

SummaryGlobal climate fluctuations have significantly influenced the distribution and abundance of biodiversity [1]. During unfavorable glacial periods, many species experienced range contraction and fragmentation, expanding again during interglacials [2–4]. An understanding of the evolutionary consequences of both historical and ongoing climate changes requires knowledge of the temporal dynamics of population numbers during such climate cycles. Variation in abundance should have left clear signatures in the patterns of intraspecific genetic variation in extant species, from which historical effective population sizes (Ne) can be estimated [3]. We analyzed whole-genome sequences of 38 avian species in a pairwise sequentially Markovian coalescent (PSMC, [5]) framework to quantitatively reveal changes in Ne from approximately 10 million to 10 thousand years ago. Significant fluctuations in Ne over time were evident for most species. The most pronounced pattern observed in many species was a severe reduction in Ne coinciding with the beginning of the last glacial period (LGP). Among species, Ne varied by at least three orders of magnitude, exceeding 1 million in the most abundant species. Several species on the IUCN Red List of Threatened Species showed long-term reduction in population size, predating recent declines. We conclude that cycles of population expansions and contractions have been a common feature of many bird species during the Quaternary period, likely coinciding with climate cycles. Population size reduction should have increased the risk of extinction but may also have promoted speciation. Species that have experienced long-term declines may be especially vulnerable to recent anthropogenic threats.

Contemporary and historic factors influence differently genetic differentiation and diversity in a tropical palm

Population genetics theory predicts loss in genetic variability because of drift and inbreeding in isolated plant populations; however, it has been argued that long-distance pollination and seed dispersal may be able to maintain gene flow, even in highly fragmented landscapes. We tested how historical effective population size, historical migration and contemporary landscape structure, such as forest cover, patch isolation and matrix resistance, affect genetic variability and differentiation of seedlings in a tropical palm (Euterpe edulis) in a human-modified rainforest. We sampled 16 sites within five landscapes in the Brazilian Atlantic forest and assessed genetic variability and differentiation using eight microsatellite loci. Using a model selection approach, none of the covariates explained the variation observed in inbreeding coefficients among populations. The variation in genetic diversity among sites was best explained by historical effective population size. Allelic richness was best explained by historical effective population size and matrix resistance, whereas genetic differentiation was explained by matrix resistance. Coalescence analysis revealed high historical migration between sites within landscapes and constant historical population sizes, showing that the genetic differentiation is most likely due to recent changes caused by habitat loss and fragmentation. Overall, recent landscape changes have a greater influence on among-population genetic variation than historical gene flow process. As immediate restoration actions in landscapes with low forest amount, the development of more permeable matrices to allow the movement of pollinators and seed dispersers may be an effective strategy to maintain microevolutionary processes.

Efficient inference of population size histories and locus-specific mutation rates from large-sample genomic variation data.

With the recent increase in study sample sizes in human genetics, there has been growing interest in inferring historical population demography from genomic variation data. Here, we present an efficient inference method that can scale up to very large samples, with tens or hundreds of thousands of individuals. Specifically, by utilizing analytic results on the expected frequency spectrum under the coalescent and by leveraging the technique of automatic differentiation, which allows us to compute gradients exactly, we develop a very efficient algorithm to infer piecewise-exponential models of the historical effective population size from the distribution of sample allele frequencies. Our method is orders of magnitude faster than previous demographic inference methods based on the frequency spectrum. In addition to inferring demography, our method can also accurately estimate locus-specific mutation rates. We perform extensive validation of our method on simulated data and show that it can accurately infer multiple recent epochs of rapid exponential growth, a signal that is difficult to pick up with small sample sizes. Lastly, we use our method to analyze data from recent sequencing studies, including a large-sample exome-sequencing data set of tens of thousands of individuals assayed at a few hundred genic regions.

Is management limiting the recovery of the New Zealand sea lion Phocarctos hookeri?

Pup production of the ‘nationally critical’ New Zealand sea lion Phocarctos hookeri has declined by 48 % since 1998, with fisheries bycatch playing a role in this decline. Current management of the sea lion population involves, amongst other measures, the setting of an annual bycatch limit based on Bayesian modelling of the sea lion population and fisheries information. Success of management scenarios is determined against two criteria, both of which involve keeping the sea lion population at or above 90 % of a modelled carrying capacity (6,987 mature individuals). Due to a lack of information on the pre-sealing abundance of the New Zealand sea lion, it is unclear whether the modelled carrying capacity represents a cap on sea lion recovery. Here, I use published estimates of genetic diversity based on microsatellite loci (expected heterozygosity, He) of the New Zealand sea lion and other otariid species to estimate historical effective population size (Ne). I then use existing knowledge of the ratio of Ne to census population size (NC) to determine a historical census population size of these species. Genetical estimates of historical Ne suggest that NZ sea lions were considerably more abundant (>68,000 individuals) historically than the current population estimate (11,855 animals). Importantly, the genetical estimate of historical population size suggests that the modelled carrying capacity (6,987 mature sea lions) is likely an underestimation of recovery potential of the species; hence, current management maybe limiting the recovery of the species.

Contrasting patterns of genetic structuring in natural populations of Arabidopsis lyrata Subsp. petraea across different regions in northern Europe.

Level and partitioning of genetic diversity is expected to vary between contrasting habitats, reflecting differences in strength of ecological and evolutionary processes. Therefore, it is necessary to consider processes acting on different time scales when trying to explain diversity patterns in different parts of species' distributions. To explore how historical and contemporary factors jointly may influence patterns of genetic diversity and population differentiation, we compared genetic composition in the perennial herb Arabidopsis lyrata ssp. petraea from the northernmost parts of its distribution range on Iceland to that previously documented in Scandinavia. Leaf tissue and soil were sampled from ten Icelandic populations of A. lyrata. Seedlings were grown from soil samples, and tissue from above-ground and seed bank individuals were genotyped with 21 microsatellite markers. Seed bank density in Icelandic populations was low but not significantly different from that observed in Norwegian populations. While within-population genetic diversity was relatively high on Iceland (H E = 0.35), among-population differentiation was low (F ST = 0.10) compared to Norwegian and Swedish populations. Population differentiation was positively associated with geographical distance in both Iceland and Scandinavia, but the strength of this relationship varied between regions. Although topography and a larger distribution range may explain the higher differentiation between mountainous Norwegian relative to lowland populations in Sweden, these factors cannot explain the lower differentiation in Icelandic compared to Swedish populations. We propose that low genetic differentiation among Icelandic populations is not caused by differences in connectivity, but is rather due to large historical effective population sizes. Thus, rather than contemporary processes, historical factors such as survival of Icelandic lineages in northern refugia during the last glacial period may have contributed to the observed pattern.

Integrating phylogeography and morphometrics to assess conservation merits and inform conservation strategies for an endangered subspecies of a common bird species

Understanding the evolutionary history of threatened populations can improve their conservation management. Re-establishment of past but recent gene flow could re-invigorate threatened populations and replenish genetic diversity, necessary for population persistence. One of the four nominal subspecies of the common yellow-tufted honeyeater, Lichenostomus melanops cassidix, is critically endangered despite substantial conservation efforts over 55years. Using a combination of morphometric, genetic and modeling approaches we tested for its evolutionary distinctiveness and conservation merit. We confirmed that cassidix has at least one morphometric distinction. It also differs genetically from the other subspecies in allele frequencies but not phylogenetically, implying that its evolution was recent. Modeling historical distribution supported a lack of vicariance and suggested possible gene flow among subspecies at least since the late Pleistocene. Multi-locus coalescent analyses indicated that cassidix diverged from its common ancestor with neighboring subspecies gippslandicus sometime from the mid-Pleistocene to the Holocene, and that it has the smallest historical effective population size of all subspecies. It appears that cassidix diverged from its ancestor with gippslandicus through a combination of drift and local selection. From patterns of genetic subdivision on two spatial scales and morphological variation we concluded that cassidix, gippslandicus and (melanops+meltoni) are diagnosable as subspecies. Low genetic diversity and effective population size of cassidix may translate to low genetic fitness and evolutionary potential, accordingly we recommend managed gene flow from gippslandicus (with which it can be inferred to have recently experienced natural gene flow) to favor recovery of cassidix.

Historical DNA reveals the demographic history of Atlantic cod (Gadus morhua) in medieval and early modern Iceland

Atlantic cod (Gadus morhua) vertebrae from archaeological sites were used to study the history of the Icelandic Atlantic cod population in the time period of 1500-1990. Specifically, we used coalescence modelling to estimate population size and fluctuations from the sequence diversity at the cytochrome b (cytb) and Pantophysin I (PanI) loci. The models are consistent with an expanding population during the warm medieval period, large historical effective population size (NE), a marked bottleneck event at 1400-1500 and a decrease in NE in early modern times. The model results are corroborated by the reduction of haplotype and nucleotide variation over time and pairwise population distance as a significant portion of nucleotide variation partitioned across the 1550 time mark. The mean age of the historical fished stock is high in medieval times with a truncation in age in early modern times. The population size crash coincides with a period of known cooling in the North Atlantic, and we conclude that the collapse may be related to climate or climate-induced ecosystem change.

Contrasting spatial genetic structure in Annona crassiflora populations from fragmented and pristine savannas

In continuous populations, fine-scale genetic structure tends to be stronger in species with restricted pollen and seed dispersal. However, habitat fragmentation and disturbances can affect genetic diversity and spatial genetic structure due to disruption in ecological processes, such as plant reproduction and seed dispersal. In this study, we compared the genetic diversity and fine-scale spatial genetic structure (SGS) in two populations of Annona crassiflora (Annonaceae) in a pristine savanna Reserve (ESECAE) and in a fragmented disturbed savanna area (PABE), both in Cerrado biome in Central Brazil. The analyses were based on the polymorphism at 10 microsatellite loci. Our working hypothesis was that SGS is stronger and genetic diversity is lower in population at fragmented area (PABE) than at pristine area (ESECAE). Both populations presented high levels of polymorphism and genetic diversity and showed no sign of bottleneck for both Wilcoxon sign-rank test for heterozygosity excess (p > 0.05) and coalescent analyses (growth parameter g not different from zero), but population at fragmented area showed higher fixation index and stronger SGS. Besides, populations are significantly differentiated (FST = 0.239, RST = 0.483, p < 0.001 for both). Coalescent analyses showed high historical effective population sizes for both populations, high gene flow between ESECAE and PABE and recent time to most recent common ancestor (~37 k year BP). Our results suggest that despite the high genetic diversity, fragmentation and disturbance may have been affecting populations of this species increasing mating between closely related individuals leading to high fixation index and strong SGS.

Linking Great Apes Genome Evolution across Time Scales Using Polymorphism-Aware Phylogenetic Models

The genomes of related species contain valuable information on the history of the considered taxa. Great apes in particular exhibit variation of evolutionary patterns along their genomes. However, the great ape data also bring new challenges, such as the presence of incomplete lineage sorting and ancestral shared polymorphisms. Previous methods for genome-scale analysis are restricted to very few individuals or cannot disentangle the contribution of mutation rates and fixation biases. This represents a limitation both for the understanding of these forces as well as for the detection of regions affected by selection. Here, we present a new model designed to estimate mutation rates and fixation biases from genetic variation within and between species. We relax the assumption of instantaneous substitutions, modeling substitutions as mutational events followed by a gradual fixation. Hence, we straightforwardly account for shared ancestral polymorphisms and incomplete lineage sorting. We analyze genome-wide synonymous site alignments of human, chimpanzee, and two orangutan species. From each taxon, we include data from several individuals. We estimate mutation rates and GC-biased gene conversion intensity. We find that both mutation rates and biased gene conversion vary with GC content. We also find lineage-specific differences, with weaker fixation biases in orangutan species, suggesting a reduced historical effective population size. Finally, our results are consistent with directional selection acting on coding sequences in relation to exonic splicing enhancers.

Genetic structure and diversity of Portunus trituberculatus in Chinese population revealed by microsatellite markers

By using six polymorphic microsatellite loci, the population genetic diversity and structure of 120 individuals of Portunus trituberculatus were examined in five wild populations representing different geographical and ecological ranges along the coast of China. Middle level of genetic diversity of P. trituberculatus was revealed by observed heterozygosity, allele number and Shannon information index. Pairwise population differentiations were found between all pairs of populations except Beihai (BH) and Qingdao (QD) (P < 0.05). The greatest differentiation was detected between Yingkou (YK) and QD populations. It was inconsistent with the result in previous study using mitochondrial control region, which showed no differentiation between QD and YK population. Recent bottleneck was identified in Ningbo (NB) population under TPM and IAM models, as well as Dandong (DD) and QD populations under IAM model. Additionally, compared with YK, QD, DD and BH populations, lower historical effective population size with lower genetic diversity were detected in NB population, which called for urgent assessment of the ecological and economic potential of NB fisheries.

Gene flow and demographic history of leopards (Panthera pardus) in the central Indian highlands.

Gene flow is a critical ecological process that must be maintained in order to counteract the detrimental effects of genetic drift in subdivided populations, with conservation benefits ranging from promoting the persistence of small populations to spreading adaptive traits in changing environments. We evaluated historical and contemporary gene flow and effective population sizes of leopards in a landscape in central India using noninvasive sampling. Despite the dramatic changes in land-use patterns in this landscape through recent times, we did not detect any signs that the leopard populations have been through a genetic bottleneck, and they appear to have maintained migration–drift equilibrium. We found that historical levels of gene flow (mean mh = 0.07) were significantly higher than contemporary levels (mean mc = 0.03), and populations with large effective population sizes (Satpura and Kanha Tiger Reserves) are the larger exporters of migrants at both timescales. The greatest decline in historical versus contemporary gene flow is between pairs of reserves that are currently not connected by forest corridors (i.e., Melghat-Pench mh − mc = 0.063; and Kanha-Satpura mh − mc = 0.054). We attribute this reduction in gene flow to accelerated fragmentation and habitat alteration in the landscape over the past few centuries, and suggest protection of forest corridors to maintain gene flow in this landscape.

Marine dispersal and barriers drive Atlantic seahorse diversification

AbstractAimTo investigate how marine barriers shaped the demographic history of Atlantic seahorses (Syngnathidae: Hippocampus).LocationAtlantic Ocean.MethodsRange‐wide sampling (n = 390) at mitochondrial and up to five nuclear DNA loci was carried out across the Hippocampus erectus species complex (H. erectus from the Caribbean/North America, H. patagonicus from South America and H. hippocampus from Europe and West Africa). Multi‐species coalescent and approximate Bayesian computation (ABC) frameworks were used to estimate support of competing biogeographical hypotheses and demographic parameters, including lineage divergence times, effective population sizes and magnitudes of population size change.ResultsWe identified four distinct lineages within the H. erectus complex. A posterior probability of 0.626 and corresponding Bayes factors ranging from 3.68 to 11.38 gave moderate to strong support for a basal divergence between South American populations of H. patagonicus and Caribbean/North American populations of H. erectus coincident with the inter‐regional freshwater outflow of the Amazon River Barrier (ARB). Estimates of historical effective population sizes and divergence times indicate that European and West African populations of H. hippocampus expanded after colonization from a more demographically stable Caribbean/North American H. erectus.Main conclusionsOur findings of trans‐Atlantic colonization followed by isolation across a deep oceanic divide, and isolation across a freshwater barrier, may demonstrate a contrast in marine divide permeability for this group of rafters. Demographic inference supports the establishment of an ancestral population of the H. erectus complex in the Americas, followed by the ARB splitting it into Caribbean/North and South American lineages at a time of increased sedimentation and outflow. Our estimates suggest that following this split, colonization occurred across the Atlantic via the Gulf Stream currents with subsequent trans‐Atlantic isolation. These results illustrate that rafting can be a means of range expansion over large distances, but may be insufficient for sustaining genetic connectivity across major barriers, thereby resulting in lineage divergence.

Insights into the evolution of Darwin’s finches from comparative analysis of the Geospiza magnirostris genome sequence

BackgroundA classical example of repeated speciation coupled with ecological diversification is the evolution of 14 closely related species of Darwin’s (Galápagos) finches (Thraupidae, Passeriformes). Their adaptive radiation in the Galápagos archipelago took place in the last 2–3 million years and some of the molecular mechanisms that led to their diversification are now being elucidated. Here we report evolutionary analyses of genome of the large ground finch, Geospiza magnirostris.Results13,291 protein-coding genes were predicted from a 991.0 Mb G. magnirostris genome assembly. We then defined gene orthology relationships and constructed whole genome alignments between the G. magnirostris and other vertebrate genomes. We estimate that 15% of genomic sequence is functionally constrained between G. magnirostris and zebra finch. Genic evolutionary rate comparisons indicate that similar selective pressures acted along the G. magnirostris and zebra finch lineages suggesting that historical effective population size values have been similar in both lineages. 21 otherwise highly conserved genes were identified that each show evidence for positive selection on amino acid changes in the Darwin's finch lineage. Two of these genes (Igf2r and Pou1f1) have been implicated in beak morphology changes in Darwin’s finches. Five of 47 genes showing evidence of positive selection in early passerine evolution have cilia related functions, and may be examples of adaptively evolving reproductive proteins.ConclusionsThese results provide insights into past evolutionary processes that have shaped G. magnirostris genes and its genome, and provide the necessary foundation upon which to build population genomics resources that will shed light on more contemporaneous adaptive and non-adaptive processes that have contributed to the evolution of the Darwin’s finches.

Genome sequencing reveals complex speciation in the Drosophila simulans clade

The three species of the Drosophila simulans clade—the cosmopolitan species, D. simulans, and the two island endemic species, D. mauritiana and D. sechellia—are important models in speciation genetics, but some details of their phylogenetic and speciation history remain unresolved. The order and timing of speciation are disputed, and the existence, magnitude, and timing of gene flow among the three species remain unclear. Here we report on the analysis of a whole-genome four-species sequence alignment that includes all three D. simulans clade species as well as the D. melanogaster reference sequence. The alignment comprises novel, paired short-read sequence data from a single highly inbred line each from D. simulans, D. mauritiana, and D. sechellia. We are unable to reject a species phylogeny with a basal polytomy; the estimated age of the polytomy is 242,000 yr before the present. However, we also find that up to 4.6% of autosomal and 2.2% of X-linked regions have evolutionary histories consistent with recent gene flow between the mainland species (D. simulans) and the two island endemic species (D. mauritiana and D. sechellia). Our findings thus show that gene flow has occurred throughout the genomes of the D. simulans clade species despite considerable geographic, ecological, and intrinsic reproductive isolation. Last, our analysis of lineage-specific changes confirms that the D. sechellia genome has experienced a significant excess of slightly deleterious changes and a dearth of presumed favorable changes. The relatively reduced efficacy of natural selection in D. sechellia is consistent with its derived, persistently reduced historical effective population size.

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.

Effective Population Size and the Efficacy of Selection on the X Chromosomes of Two Closely Related Drosophila Species

The prevalence of natural selection relative to genetic drift is of central interest in evolutionary biology. Depending on the distribution of fitness effects of new mutations, the importance of these evolutionary forces may differ in species with different effective population sizes. Here, we survey population genetic variation at 105 orthologous X-linked protein coding regions in Drosophila melanogaster and its sister species D. simulans, two closely related species with distinct demographic histories. We observe significantly higher levels of polymorphism and evidence for stronger selection on codon usage bias in D. simulans, consistent with a larger historical effective population size on average for this species. Despite these differences, we estimate that <10% of newly arising nonsynonymous mutations have deleterious fitness effects in the nearly neutral range (i.e., −10 < Nes < 0) in both species. The inferred distributions of fitness effects and demographic models translate into surprisingly high estimates of the fraction of “adaptive” protein divergence in both species (∼85–90%). Despite evidence for different demographic histories, differences in population size have apparently played little role in the dynamics of protein evolution in these two species, and estimates of the adaptive fraction (α) of protein divergence in both species remain high even if we account for recent 10-fold growth. Furthermore, although several recent studies have noted strong signatures of recurrent adaptive protein evolution at genes involved in immunity, reproduction, sexual conflict, and intragenomic conflict, our finding of high levels of adaptive protein divergence at randomly chosen proteins (with respect to function) suggests that many other factors likely contribute to the adaptive protein divergence signature in Drosophila.

Linkage disequilibrium and historical effective population size in the Thoroughbred horse

Many genomic methodologies rely on the presence and extent of linkage disequilibrium (LD) between markers and genetic variants underlying traits of interest, but the extent of LD in the horse has yet to be comprehensively characterized. In this study, we evaluate the extent and decay of LD in a sample of 817 Thoroughbreds. Horses were genotyped for over 50,000 single nucleotide polymorphism (SNP) markers across the genome, with 34,848 autosomal SNPs used in the final analysis. Linkage disequilibrium, as measured by the squared correlation coefficient (r(2)), was found to be relatively high between closely linked markers (>0.6 at 5 kb) and to extend over long distances, with average r(2) maintained above non-syntenic levels for single nucleotide polymorphisms (SNPs) up to 20 Mb apart. Using formulae which relate expected LD to effective population size (N(e)), and assuming a constant actual population size, N(e) was estimated to be 100 in our population. Values of historical N(e), calculated assuming linear population growth, suggested a decrease in N(e) since the distant past, reaching a minimum twenty generations ago, followed by a subsequent increase until the present time. The qualitative trends observed in N(e) can be rationalized by current knowledge of the history of the Thoroughbred breed, and inbreeding statistics obtained from published pedigree analyses are in agreement with observed values of N(e). Given the high LD observed and the small estimated N(e), genomic methodologies such as genomic selection could feasibly be applied to this population using the existing SNP marker set.

Range-wide mtDNA phylogeography yields insights into the origins of Asian elephants

Range-wide mtDNA phylogeography yields insights into the origins of Asian elephants