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Estimating population structure under nonequilibrium conditions in a conservation context: continent-wide population genetics of the giant Amazon river turtle, Podocnemis expansa (Chelonia; Podocnemididae).

Giant Amazon river turtles, Podocnemis expansa, are indigenous to the Amazon, Orinoco, and Essequibo River basins, and are distributed across nearly the entire width of the South American continent. Although once common, their large size, high fecundity, and gregarious nesting, made P. expansa especially vulnerable to over-harvesting for eggs and meat. Populations have been severely reduced or extirpated in many areas throughout its range, and the species is now regulated under Appendix II of the Convention on International Trade in Endangered Species. Here, we analyse data from mitochondrial DNA sequence and multiple nuclear microsatellite markers with an array of complementary analytical methods. Results show that concordance from multiple data sets and analyses can provide a strong signal of population genetic structure that can be used to guide management. The general lack of phylogeographic structure but large differences in allele and haplotype frequencies among river basins is consistent with fragmented populations and female natal-river homing. Overall, the DNA data show that P. expansa populations lack a long history of genetic differentiation, but that each major tributary currently forms a semi-isolated reproductive population and should be managed accordingly.

Animals↗

Serogenetic analysis in the study of the population structure of the eastern Adriatic (Croatia).

The anthropogenetic structure of six island and peninsular populations (Brac, Hvar, Korcula, Peljesac, Silba, and Olib) of the eastern Adriatic, Croatia, is analyzed on the basis of the study of four different erythrocyte antigen systems or groups (ABO, Rhesus, Kell-Celano, P) and two erythrocyte isoenzyme systems (ACP, ESD). The average sample size was 555 individuals. Allele frequencies, genetic distances, and gene diversity values were computed. The results indicate that all the populations in question have preserved their separate characteristics over the course of their (micro)evolution to the present day; this is especially noticeable for the island populations of Korcula and Olib, as these are distinguished from the other four populations by a greater degree of isolation. Today's genetic structure of the six populations can be explained through the existing historical and cultural data for the region in question, which indicate that over the course of their ethnohistory they were all influenced by significant waves of immigration and selective emigrations that must have greatly shaped their present-day population structure.

Alleles↗

Globalization and the population structure of Toxoplasma gondii.

Toxoplasma gondii is a protozoan parasite that infects nearly all mammal and bird species worldwide. Usually asymptomatic, toxoplasmosis can be severe and even fatal to many hosts, including people. Elucidating the contribution of genetic variation among parasites to patterns of disease transmission and manifestations has been the goal of many studies. Focusing on the geographic component of this variation, we show that most genotypes are locale-specific, but some are found across continents and are closely related to each other, indicating a recent radiation of a pandemic genotype. Furthermore, we show that the geographic structure of T. gondii is extraordinary in having one population that is found in all continents except South America, whereas other populations are generally confined to South America, and yet another population is found worldwide. Our evidence suggests that South American and Eurasian populations have evolved separately until recently, when ships populated by rats, mice, and cats provided T. gondii with unprecedented migration opportunities, probably during the transatlantic slave trade. Our results explain several enigmatic features of the population structure of T. gondii and demonstrate how pervasive, prompt, and elusive the impact of human globalization is on nature.

Animals↗

Larval Genomics as a Viable, Fisheries-Independent Tool for Investigating Population Structure in Tropical Pacific Tunas.

Understanding how dispersal, life history, and environmental variability shape genetic connectivity in the open ocean remains a central challenge in evolutionary biology. Highly migratory marine predators like tunas have traditionally been considered genetically homogeneous across ocean basins, yet emerging genomic evidence suggests that cryptic population structure can persist even in species with high gene flow and large effective population sizes. We used 2bRAD sequencing of 348 larval and subadult skipjack (Katsuwonus pelamis), yellowfin (Thunnus albacares), and bigeye tuna (T. obesus) collected from the central Pacific across 7 years of sampling to examine species boundaries, population genetic information, genetic structure, and connectivity. Larval sampling revealed consistent spawning by all three species and enabled unbiased detection of genetic patterns prior to recruitment bottlenecks. We found strong divergence amongst species, no evidence of structuring within skipjack or bigeye, and a divergent yellowfin population detected in 2 consecutive sampling years north of American Samoa. Comparisons between larvae and subadults suggest that sampling early life history stages can be a valuable tool for assessing population genetic information before recruitment bottlenecks, selective harvest by fisheries, adult dispersal, and selective pressures acting on adult populations, thereby contributing novel insights to the research and effective management of these species. These results highlight how larval genomics can complement traditional population genomic studies of adult tunas and reveal fine-scale structure in highly vagile species, providing new perspectives on connectivity in the open ocean.

Animals↗

Detecting inbreeding depression in structured populations.

Measuring inbreeding and its consequences on fitness is central for many areas in biology including human genetics and the conservation of endangered species. However, there is no consensus on the best method, neither for quantification of inbreeding itself nor for the model to estimate its effect on specific traits. We simulated traits based on simulated genomes from a large pedigree and empirical whole-genome sequences of human data from populations with various sizes and structures (from the 1,000 Genomes project). We compare the ability of various inbreeding coefficients ([Formula: see text]) to quantify the strength of inbreeding depression: allele-sharing, two versions of the correlation of uniting gametes which differ in the weight they attribute to each locus and two identical-by-descent segments-based estimators. We also compare two models: the standard linear model and a linear mixed model (LMM) including a genetic relatedness matrix (GRM) as random effect to account for the nonindependence of observations. We find LMMs give better results in scenarios with population or family structure. Within the LMM, we compare three different GRMs and show that in homogeneous populations, there is little difference among the different [Formula: see text] and GRM for inbreeding depression quantification. However, as soon as a strong population or family structure is present, the strength of inbreeding depression can be most efficiently estimated only if i) the phenotypes are regressed on [Formula: see text] based on a weighted version of the correlation of uniting gametes, giving more weight to common alleles and ii) with the GRM obtained from an allele-sharing relatedness estimator.

Humans↗

The study of structured populations--new hope for a difficult and divided science.

Natural populations, including those of humans, have complex geographies and histories. Studying how they evolve is difficult, but it is possible with population-based DNA sequence data. However, the study of structured populations is divided by two distinct schools of thought and analysis. The phylogeographic approach is fundamentally graphical and begins with a gene-tree estimate. By contrast, the more traditional approach of using summary statistics is fundamentally mathematical. Both approaches have limitations, but there is promise in newer probabilistic methods that offer the flexibility and data exploitation of the phylogeographic approach in an explicitly model-based mathematical framework.

Animals↗

Cytochrome b polymorphisms and population structure of two species of Alouatta (Primates).

We carried out a phylogenetic and population study in Alouatta caraya and Alouatta belzebul based on cytochrome b DNA sequence data. Maximum Parsimony and Median-Joining analyses grouped A. caraya from different localities showing a population structure in accordance with geographic distribution. The relation between A. caraya haplotypes could be explained with respect to the species range in the Cerrado, one of the most ancient morphoclimatic domains of South America, and the Chaco. Conversely, A. belzebul from the Amazonas and Atlantic forests grouped in a paraphyletic arrangement without an evident geographic pattern. Recent geologic events resulting in the separation of A. belzebul might explain why these geographically distant groups shared similar haplotypes and why ancestral polymorphisms might have been maintained in this species. Time of divergence estimates indicated that the splitting of the Alouatta lineage leading to A. caraya occurred some 4.58 MYA while the lineage leading to A. belzebul emerged 4.14 MYA.

Alouatta↗

Cobitis ohridana and Barbatula zetensis in the River Moraca basin, Montenegro: distribution, habitat, population structure and conservation needs.

In this paper, we report on the distribution, habitat, population structure and conservation needs of Cobitis ohridana and Barbatula zetensis in the basin of the River Moraca in Montenegro. Our data show both species to be mainly distributed in the lower stretch of the main river and some tributaries in lowland habitats. Cobitis ohridana preferred more shallow water with a higher abundance of filamentous algae, while Barbatula zetensis was more numerous in slightly deeper water with more stones as a bottom substrate. Slight differences in the habitat preference were also observed between juveniles and adults in both species. Although both species are abundant in suited habitat, they have a small distribution area in the Moraca basin due to the natural rarity of the habitat. According to our data, they are not endangered.

Animals↗

Population structure of Plasmodium falciparum isolates during an epidemic in southern Mauritania.

While the population structure of Plasmodium falciparum is well analysed in selected areas with high malaria endemicity in East and West Africa, only limited data are available for low endemicity regions bordering the Saharan desert. This is one of the first studies for the Sahel, where atypically strong rainfalls in 1998 and 1999 led to a severe outbreak of falciparum malaria in south-east Mauritania. During a study on in vivo-drug resistance against chloroquine we collected blood samples of patients with fever in two medical centres located in non-endemic and hypoendemic areas. We analysed 386 samples by polymerase chain reaction for infection with P. falciparum, and 173 (45%) tested positive. The isolates were genotyped for three polymorphic genetic markers: merozoite surface protein 1 (MSP1), MSP2 and glutamate-rich protein (GLURP). Differences between the two regions could be shown in either number of clones per infection or in their distribution on the different allelic groups. While the mean minimal number of clones in the non-endemic region around Aioun was 1.57, blood samples collected in the hypoendemic region around Kobeni showed multiple infections with an average of 2.34 clones (P < 0.001). In addition, clear differences between endemic regions were apparent in three of the investigated allelic groups: RO33 of the MSP1 gene and FC and Indochina of the MSP2 gene.

Adolescent↗

Spatial epidemiology and natural population structure of Campylobacter jejuni colonizing a farmland ecosystem.

Recent progress in determining the population structure of Campylobacter jejuni, and discerning associations between genotypes and specific niches, has emphasized the shortfall in our understanding of the ecology and epidemiology of this bacterium. We examined the natural structure of the C. jejuni community associated with cattle farmland in the UK by structured spatiotemporal sampling of habitats, including livestock and wild animal faeces, environmental water and soil, over a 10-week period within a 100 km2 area. A total of 172 isolates were characterized using multilocus sequence typing into 65 sequence types (STs). Isolates from cattle faeces were significantly over-represented in the ST-61 complex, whereas isolates from wildlife faeces and water were more likely to belong to the ST-45 complex and a number of unusual STs, many of which were first encountered during this study. Sampling within a narrow spatiotemporal window permitted the application of novel statistical methods exploring the relationship between the genetic relatedness and spatial separation of isolates. This approach showed that isolates from the same sampling squares and squares separated by <1.0 km were genetically more similar than isolates separated by greater distances. Our study demonstrates the potential of multilocus sequence typing combined with spatial modelling in exploring natural transmission pathways for C. jejuni.

Agriculture↗

Population structure of Anisakis simplex (Nematoda) in harbor porpoises Phocoena phocoena off Denmark.

The population structure and habitat selection of Anisakis simplex in 35 harbor porpoises off Denmark are described. The nematodes were collected from the stomach and duodenal ampulla and were categorized as third-stage larvae, fourth-stage larvae, subadults, and adults. The porpoises harbored 8,043 specimens of A. simplex. The proportion of adults and subadults increased with infrapopulation size. The number of development stages across infrapopulations covaried significantly (Kendall's test of concordance). Concordance was higher in hosts with the highest intensities than in those with low and medium intensities. All stages occurred mainly in the forestomach, but this trend was stronger for the adults. Adult and subadult sex ratios did not depart significantly from 1:1. Our data suggested that recruitment and duration of each stage were the main factors accounting for infrapopulation structure. The preference of A. simplex for the forestomach conformed with previous studies, but the narrower distribution of adults relative to other stages might indicate a strategy to enhance mating opportunities. Information on sex ratios of A. simplex is scarce and contradictory. We suggest that the discrepancies might partly reflect differences in categorization criteria and statistical methods.

Animals↗

Inferring a population structure for Staphylococcus epidermidis from multilocus sequence typing data.

Despite its importance as a human pathogen, information on population structure and global epidemiology of Staphylococcus epidermidis is scarce and the relative importance of the mechanisms contributing to clonal diversification is unknown. In this study, we addressed these issues by analyzing a representative collection of S. epidermidis isolates from diverse geographic and clinical origins using multilocus sequence typing (MLST). Additionally, we characterized the mobile element (SCCmec) carrying the genetic determinant of methicillin resistance. The 217 S. epidermidis isolates from our collection were split by MLST into 74 types, suggesting a high level of genetic diversity. Analysis of MLST data using the eBURST algorithm revealed the existence of nine epidemic clonal lineages that were disseminated worldwide. One single clonal lineage (clonal complex 2) comprised 74% of the isolates, whereas the remaining isolates were clustered into 8 minor clonal lineages and 13 singletons. According to our evolutionary model, SCCmec was acquired at least 56 times by S. epidermidis. Although geographic dissemination of S. epidermidis strains and the value of the index of association between the alleles, 0.2898 (P < 0.05), support the clonality of S. epidermidis species, examination of the sequence changes at MLST loci during clonal diversification showed that recombination gives rise to new alleles approximately twice as frequently as point mutations. We suggest that S. epidermidis has a population with an epidemic structure, in which nine clones have emerged upon a recombining background and evolved quickly through frequent transfer of genetic mobile elements, including SCCmec.

Algorithms↗

Population structure delineated with microsatellite markers in fragmented populations of a tropical tree, carapa guianensis (Meliaceae)

Deforestation and selective logging in the tropics may have serious consequences on genetic processes in tropical tree populations, affecting long-term survival of a given species as well as tropical forest communities. Because understanding the effects of human-induced changes on genetic processes is of utmost importance in formulating sound conservation and management plans for tropical forest communities, we developed microsatellite or simple sequence repeat (SSR) markers for the tropical tree Carapa guianensis (Meliaceae) and assessed the polymorphism of SSRs in adult and sapling populations in a large contiguous forest and in selectively logged and fragmented forests. The number of alleles in polymorphic loci ranged between 4 and 28. No inbreeding was detected in saplings or adult cohorts, but the allelic richness was lower in the sapling cohort of the isolated fragment. Genetic distances, Nei's D and (delta&mgr;)2, and RST values among saplings were greater than among adult cohorts, suggesting restriction of gene flow due to deforestation and habitat fragmentation. These SSR loci may be used to address many related questions regarding the population and conservation genetics of tropical trees.

Journal Article↗

Microsatellite analysis of population structure and genetic differentiation within and between populations of the root vole, Microtus oeconomus in the Netherlands.

Eight microsatellite markers for the root vole (Microtus oeconomus) were developed to assess the amount of genetic variation for nine Dutch root vole populations from four different regions, and to evaluate the degree of differentiation and isolation. All eight microsatellite loci were found to be highly variable with observed heterozygosity values ranging from 0.61 to 0.82. These values are similar to those observed for more distant populations from Norway, Finland and Germany. Therefore, the populations seem not particularly depauperate of genetic variation at the microsatellite level. Genetically, the Dutch populations were found to have diverged considerably. Pairwise comparisons of all populations studied revealed FST values significantly greater than zero for most comparisons. However, the magnitude of these values considerably depends on the compared population pair. The level of differentiation between local populations within Dutch regions is generally significantly lower than the differentiation between Dutch regions. The level of differentiation between Dutch regions, however, is not significantly different from that between populations of larger geographical distance. This implies that the regional Dutch populations are both isolated from each other and from other European populations. The observation that even local populations show low but significant genetic differentiation may be indicative for progressive isolation of these populations.

Animals↗

Population structure in a critically endangered arctic fox population: does genetics matter?

The arctic fox (Alopex lagopus) in Scandinavia is classified as critically endangered after having gone through a severe decline in population size in the beginning of the 20th century, from which it has failed to recover despite more than 65 years of protection. Arctic foxes have a high dispersal rate and often disperse over long distances, suggesting that there was probably little population differentiation within Scandinavia prior to the bottleneck. It is, however, possible that the recent decline in population size has led to a decrease in dispersal and an increase in population fragmentation. To examine this, we used 10 microsatellite loci to analyse genetic variation in 150 arctic foxes from Scandinavia and Russia. The results showed that the arctic fox in Scandinavia presently is subdivided into four populations, and that the Kola Peninsula and northwest Russia together form a large fifth population. Current dispersal between the populations seemed to be very low, but genetic variation within them was relatively high. This and the relative F(ST) values among the populations are consistent with a model of recent fragmentation within Scandinavia. Since the amount of genetic variation is high within the populations, but the populations are small and isolated, demographic stochasticity seems to pose a higher threat to the populations' persistence than inbreeding depression and low genetic variation.

Alleles↗

Consequences of population structure on genes under balancing selection.

This paper describes a new approach to modeling population structure for genes under strong balancing selection of the type seen in plant self-incompatibility systems and the major histocompatibility complex (MHC) system of vertebrates. Simple analytic solutions for the number of alleles maintained at equilibrium and the expected proportion of alleles shared between demes at various levels are derived and checked against simulation results. The theory accurately captures the dynamics of allele number in a subdivided population and identifies important values of m (migration rate) at which allele number and distribution change qualitatively. Starting from a panmictic population, as migration among demes decreases a qualitative change in dynamics is seen at approximately m(crit) approximately equal to the square root of(s/4piNT) where NT is the total population size and s is a measure of the strength of selection. At this point, demes can no longer maintain their panmictic allele number, due to increasing isolation from the total population. Another qualitative change occurs at a migration rate on the same order of magnitude as the mutation rate, mu. At this point, the demes are highly differentiated for allele complement, and the total number of alleles in the population is increased. Because in general u << m<(crit) at intermediate migration rates slightly fewer alleles may be maintained in the total population than are maintained at panmixia. Within this range, total allele number may not be the best indicator of whether a population is effectively panmictic, and some caution should be used when interpreting samples from such populations. The theory presented here can help to analyze data from genes under balancing selection in subdivided populations.

Alleles↗

Congruent epidemic models for unstructured and structured populations: analytical reconstruction of a 2003 SARS outbreak.

Both the threat of bioterrorism and the natural emergence of contagious diseases underscore the importance of quantitatively understanding disease transmission in structured human populations. Over the last few years, researchers have advanced the mathematical theory of scale-free networks and used such theoretical advancements in pilot epidemic models. Scale-free contact networks are particularly interesting in the realm of mathematical epidemiology, primarily because these networks may allow meaningfully structured populations to be incorporated in epidemic models at moderate or intermediate levels of complexity. Moreover, a scale-free contact network with node degree correlation is in accord with the well-known preferred mixing concept. The present author describes a semi-empirical and deterministic epidemic modeling approach that (a) focuses on time-varying rates of disease transmission in both unstructured and structured populations and (b) employs probability density functions to characterize disease progression and outbreak controls. Given an epidemic curve for a historical outbreak, this modeling approach calls for Monte Carlo calculations (that define the average new infection rate) and solutions to integro-differential equations (that describe outbreak dynamics in an aggregate population or across all network connectivity classes). Numerical results are obtained for the 2003 SARS outbreak in Taiwan and the dynamical implications of time-varying transmission rates and scale-free contact networks are discussed in some detail.

Disease Outbreaks↗

Population structure of wild bananas, Musa balbisiana, in China determined by SSR fingerprinting and cpDNA PCR-RFLP.

Both demographic history and dispersal mechanisms influence the apportionment of genetic diversity among plant populations across geographical regions. In this study, phylogeography and population structure of wild banana, Musa balbisiana, one of the progenitors of cultivated bananas and plantains in China were investigated by an analysis of genetic diversity of simple sequence repeat (SSR) fingerprint markers and cpDNA PCR-RFLP. A chloroplast DNA (cpDNA) genealogy of 21 haplotypes identified two major clades, which correspond to two geographical regions separated by the Beijiang and Xijiang rivers, suggesting a history of vicariance. Significant genetic differentiation was detected among populations with cpDNA markers, a result consistent with limited seed dispersal in wild banana mediated by foraging of rodents. Nuclear SSR data also revealed significant geographical structuring in banana populations. In western China, however, there was no detected phylogeograpahical pattern, possibly due to frequent pollen flow via fruit bats. In contrast, populations east of the Beijiang River and the population of Hainan Island, where long-range soaring pollinators are absent, are genetically distinct. Colonization-extinction processes may have influenced the evolution of Musa populations, which have a metapopulation structure and are connected by migrating individuals. Effective gene flow via pollen, estimated from the nuclear SSR data, is 3.65 times greater than gene flow via seed, estimated from cpDNA data. Chloroplast and nuclear DNAs provide different insights into phylogeographical patterns of wild banana populations and, taken together, can inform conservation practices.

China↗