Mitochondrial DNA variation in the malaria vector Anopheles minimus across China,Thailand and Vietnam: evolutionary hypothesis,population structure and population history

The effects of Pleistocene environmental fluctuations on the distribution and diversity of organisms in Southeast Asia are much less well known than in Europe and North America. In these regions, the combination of palaeoenvironmental reconstruction and inferences about population history from genetic data has been very powerful. In Southeast Asia, mosquitoes are good candidates for the genetic approach, with the added benefit that understanding the relative contributions of historical and current processes to population structure can inform management of vector species. Genetic variation among populations of Anopheles minimus was examined using 144 mtDNA COII sequences from 23 sites in China, Thailand and Vietnam. Haplotype diversity was high, with two distinct lineages that have a sequence divergence of over 2% and exhibit different geographical distributions. We compare alternative hypotheses concerning the origin of this pattern. The observed data deviate from the expectations based on a single-panmictic population with or without growth, or a stable but spatially structured population. However, they can be readily accommodated by a model of past fragmentation into eastern and western refugia, followed by growth and range expansion. This is consistent with the palaeoenvironmental reconstructions currently available for the region.     

Microevolution of the Chibcha-speaking peoples of lower Central America: rare genes in an Amerindian complex.

Models are developed for the survival, history, and spread of variant alleles, in order to consider what can, and what cannot, be inferred from this type of data. The high variances of the processes involved, and questions of sampling, place severe limitations on inferences. Nonetheless, by combining information on a number of rare variants observed in a group of interrelated populations, reliable qualitative inferences are possible. These ideas and models are developed in the context of data on five rare variants and six private polymorphisms observed in eight Chibcha-speaking tribes of Costa Rica and Panama. The decline and fragmentation of the Amerindian populations of Central America over the last 300 years create considerable difficulties in attempting inference of past genetic events. However, these tribes have been well studied genetically, anthropologically, and linguistically and thus provide an excellent framework for the study of rare-variant spread.     

Neutral and functionally important genes shed light on phylogeography and the history of high‐altitude colonization in a widespread New World duck

Phylogeographic studies often infer historical demographic processes underlying species distributions based on patterns of neutral genetic variation, but spatial variation in functionally important genes can provide additional insights about biogeographic history allowing for inferences about the potential role of adaptation in geographic range evolution. Integrating data from neutral markers and genes involved in oxygen (O₂)‐transport physiology, we test historical hypotheses about colonization and gene flow across low‐ and high‐altitude regions in the Ruddy Duck (Oxyura jamaicensis), a widely distributed species in the New World. Using multilocus analyses that for the first time include populations from the Colombian Andes, we also examined the hypothesis that Ruddy Duck populations from northern South America are of hybrid origin. We found that neutral and functional genes appear to have moved into the Colombian Andes from both North America and southern South America, and that high‐altitude Colombian populations do not exhibit evidence of adaptation to hypoxia in hemoglobin genes. Therefore, the biogeographic history of Ruddy Ducks is likely more complex than previously inferred. Our new data raise questions about the hypothesis that adaptation via natural selection to high‐altitude conditions through amino acid replacements in the hemoglobin protein allowed Ruddy Ducks to disperse south along the high Andes into southern South America. The existence of shared genetic variation with populations from both North America and southern South America as well as private alleles suggests that the Colombian population of Ruddy Ducks may be of old hybrid origin. This study illustrates the breadth of inferences one can make by combining data from nuclear and functionally important loci in phylogeography, and underscores the importance of complete range‐wide sampling to study species history in complex landscapes.     

Bayesian statistical treatment of the fluorescence of AFLP bands leads to accurate genetic structure inference

Ever since the introduction of allozymes in the 1960s, evolutionary biologists and ecologists have continued to search for more powerful molecular markers to estimate important parameters such as effective population size and migration rates and to make inferences about the demographic history of populations, the relationships between individuals and the genetic architecture of phenotypic variation (Bensch & Akesson 2005; Bonin et al. 2007). Choosing a marker requires a thorough consideration of the trade-offs associated with the different techniques and the type of data obtained from them. Some markers can be very informative but require substantial amounts of start-up time (e.g. microsatellites), while others require very little time but are much less polymorphic. Amplified fragment length polymorphism (AFLP) is a firmly established molecular marker technique that falls in this latter category. AFLPs are widely distributed throughout the genome and can be used on organisms for which there is no a priori sequence information (Meudt & Clarke 2007). These properties together with their moderate cost and short start-up time have made them the method of choice for many molecular ecology studies of wild species (Bensch & Akesson 2005). However, they have a major disadvantage, they are dominant. This represents a very important limitation because many statistical genetics methods appropriate for molecular ecology studies require the use of codominant markers. In this issue, Foll et al. (2010) present an innovative hierarchical Bayesian method that overcomes this limitation. The proposed approach represents a comprehensive statistical treatment of the fluorescence of AFLP bands and leads to accurate inferences about the genetic structure of natural populations. Besides allowing a quasi-codominant treatment of AFLPs, this new method also solves the difficult problems posed by subjectivity in the scoring of AFLP bands.     

Dynamics of genets in cluonal plants

Processes related to dispersal, recruitment and survivorship of 'genetic individuals' in clonal plants have long been considered enigmatic. Little is known of whole life-cycle dynamics in these, usually, very long-lived plants. However, inferences may be drawn from studies of specific aspects of clonal plant populations, in particular seedling recruitment, genetic structure and growth form variation. This review summarizes recent findings from such studies, and presents some conclusions concerning genet population structure and regulation, and life history evolution in clonal plants.     

Human populations show reduced DNA sequence variation at the factor IX locus

Levels and patterns of human DNA sequence variation vary widely among loci. However, some of this variation may be due to the different populations used in different studies. So far, few studies of diverse human populations have compared different genetic loci for the same samples of populations and individuals. Here, we present new polymorphism data from intron 4 of the Factor IX gene (FIX) sequenced in diverse Old World populations. An explicit comparison is made with another X-linked gene, PDHA1, for which the sampling of individuals was very similar. Despite having a similar amount of divergence from chimpanzees, as do other nuclear genes, FIX has comparatively much less DNA sequence variation among humans. Nucleotide diversity at FIX is the lowest among the existing non-Y chromosome nuclear gene datasets and is less than 10% of the diversity found at PDHA1. Estimates of effective population size based on FIX are 8,558, about half of the value obtained for PDHA1, and the time to the most recent common ancestry among human FIX gene copies (282,000 years) is one of the most recent estimates reported for human genes. Analyses presented here suggest a history for the FIX region that includes recent positive directional selection, or background, selection. The general conclusion emerging is that very large variations can exist between the histories of similar genomic regions, even when sampling differences are minimized.     

Landscape genetics in a changing world: disentangling historical and contemporary influences and inferring change

Landscape genetics seeks to determine the effect of landscape features on gene flow and genetic structure. Often, such analyses are intended to inform conservation and management. However, depending on the many factors that influence the time to reach equilibrium, genetic structure may more strongly represent past rather than contemporary landscapes. This well‐known lag between current demographic processes and population genetic structure often makes it challenging to interpret how contemporary landscapes and anthropogenic activity shape gene flow. Here, we review the theoretical framework for factors that influence time lags, summarize approaches to address this temporal disconnect in landscape genetic studies, and evaluate ways to make inferences about landscape change and its effects on species using genetic data alone or in combination with other data. Those approaches include comparing correlation of genetic structure with historical versus contemporary landscapes, using molecular markers with different rates of evolution, contrasting metrics of genetic structure and gene flow that reflect population genetic processes operating at different temporal scales, comparing historical and contemporary samples, combining genetic data with contemporary estimates of species distribution or movement, and controlling for phylogeographic history. We recommend using simulated data sets to explore time lags in genetic structure, and argue that time lags should be explicitly considered both when designing and interpreting landscape genetic studies. We conclude that the time lag problem can be exploited to strengthen inferences about recent landscape changes and to establish conservation baselines, particularly when genetic data are combined with other data.     

Heritability and evolvability of fitness and nonfitness traits: Lessons from livestock

Data from natural populations have suggested a disconnection between trait heritability (variance standardized additive genetic variance, V_A) and evolvability (mean standardized V_A) and emphasized the importance of environmental variation as a determinant of trait heritability but not evolvability. However, these inferences are based on heterogeneous and often small datasets across species from different environments. We surveyed the relationship between evolvability and heritability in >100 traits in farmed cattle, taking advantage of large sample sizes and consistent genetic approaches. Heritability and evolvability estimates were positively correlated (r = 0.37/0.54 on untransformed/log scales) reflecting a substantial impact of V_A on both measures. Furthermore, heritabilities and residual variances were uncorrelated. The differences between this and previously described patterns may reflect lower environmental variation experienced in farmed systems, but also low and heterogeneous quality of data from natural populations. Similar to studies on wild populations, heritabilities for life‐history and behavioral traits were lower than for other traits. Traits having extremely low heritabilities and evolvabilities (17% of the studied traits) were almost exclusively life‐history or behavioral traits, suggesting that evolutionary constraints stemming from lack of genetic variability are likely to be most common for classical “fitness” (cf. life‐history) rather than for “nonfitness” (cf. morphological) traits.     

Factors influencing intraspecific variation and polymorphism in marine podocopid Ostracoda,with particular reference to Tertiary species from southeastern Australia

Work on intraspecific variation in ornate ostracods over the last 30 years is reviewed. Polymorphism (discontinuous variation) due to environmental and genetic factors (and combinations thereof) is discussed. Specimens of the ornate marine genera Cletocythereis, Hermanites, Notocarinovalva, Neobuntonia, Chapmanella, Actinocythereis, Spinobradleya and Loxoconcha, from Tertiary deposits of southeastern Australia, are examined for examples of significant intraspecific morphological variation. Variations in the degree of spinosity, the nature of spines, the degree and type of aggradation (celation), the occurrence of microreticulation, the shape of fossae, the form of eye tubercles and subcentral tubercles, combinations of reticulation and nodules, and the relationships between punctation, reticulation and spinosity, are described and illustrated. These variations are considered in relation to location, time, facies, inferred palaeoenvironment and assemblage. It is shown that the complex of factors connecting these variations with their expression by the phenotype does not allow their unqualified use in establishing palaeoecological parameters, especially where strict polymorphism is not established, or where the timescale of the variations may be several orders of magnitude out of step with the palaeoecological changes inferred from them. The necessity of high magnification illustrations is stressed. The entire range of research into intraspecific variation must be accessed if robust palaeoecological inferences are to be drawn.     

Evolution of balanced genetic polymorphism

Extreme genetic polymorphism maintained by balancing selection (so called because many alleles are maintained in a balance by a mechanism of rare allele advantage) is intimately associated with the important task of self/non-self-discrimination. Widely disparate self-recognition systems of plants, animals and fungi share several general features, including the maintenance of large numbers of alleles at relatively even frequency, and persistence of this variation over very long time periods. Because the evolutionary dynamics of balanced polymorphism are very different from those of neutral genetic variation, data on balanced polymorphism have been used as a novel source for inference of the history of populations. This review highlights the unique evolutionary properties of balanced genetic polymorphism, and the use of theoretical understanding in analysis and application of empirical data for inference of population history. However, a second goal of this review is to point out where current theory is incomplete. Recent observations suggest that entirely novel selective forces may act in concert with balancing selection, and these novel forces may be extremely potent in shaping genetic variation at self-recognition loci.     

A multi-locus assessment of connectivity and historical demography in the bluehead wrasse (Thalassoma bifasciatum)

The pelagic larval stage of most coral reef fishes might allow extensive dispersal or, alternatively, some level of local recruitment might be important. Molecular markers can be used to obtain indirect estimates of dispersal to evaluate these alternatives, yet the extent of gene flow among populations is known for only a small number of species. The use of such markers must take into account the properties of the markers and the demographic history of the population when making inferences about current gene flow. In the Caribbean bluehead wrasse, Thalassoma bifasciatum, previous studies have found both substantial levels of local recruitment, in studies interpreting otolith microchemistry and, conversely, a lack of genetic differentiation inferred from mitochondrial DNA (mtDNA) restriction-fragment length polymorphism (RFLP) data and allozymes. However, if subtle differentiation exists, larger sample sizes and highly variable markers may be required to discern it. Here we present results from mitochondrial control region sequence and microsatellite data that indicate a lack of genetic differentiation at both small and large spatial scales. However, historical processes, such as changes in population size, may have affected the current distribution of genetic variation.     

Genetics of recent habitat contraction and reduction in population size: does isolation by distance matter?

Fragmentation and loss of natural habitats are recognized as major threats to contemporary flora and fauna. Detecting past or current reductions in population size is therefore a major aim in conservation genetics. Statistical methods developed to this purpose have tended to ignore the effects of spatial population structure. However in many species, individual dispersal is restricted in space and fine-scale spatial structure such as isolation by distance (IBD) is commonly observed in continuous populations. Using a simulation-based approach, we investigated how comparative and single-point methods, traditionally used in a Wright-Fisher (WF) population context for detecting population size reduction, behave for IBD populations. We found that a complex 'quartet' of factors was acting that includes restricted dispersal, population size (i.e. habitat size), demographic history, and sampling scale. After habitat reduction, IBD populations were characterized by a stronger inertia in the loss of genetic diversity than WF populations. This inertia increases with the strength of IBD, and decreases when the sampling scale increases. Depending on the method used to detect a population size reduction, a local sampling can be more informative than a sample scaled to habitat size or vice versa. However, IBD structure led in numerous cases to incorrect inferences on population demographic history. The reanalysis of a real microsatellite data set of skink populations from fragmented and intact rainforest habitats confirmed most of our simulation results.     

DNA polymorphism in a worldwide sample of human X chromosomes

DNA sequence data from humans can provide insight into the history of modern humans and the genetic variability in human populations. We report here a study of human DNA sequence variation at an X-linked noncoding region of 10,346 bp. The sample consists of 62 X chromosomes from Africa, Europe, and Asia. Forty-four polymorphic sites were found among the 62 sequences, resulting in 23 different haplotypes. Statistical analyses of the data led to the following inferences. (1) There is strong evidence of human population expansion in the relatively recent past, and this population expansion has had a significant effect on the pattern of polymorphism at this locus. (2) Non-African populations were unlikely to have been derived from a very small number of African lineages. (3) There was considerable geographic subdivision in the ancient human population, which could be an important reason why many studies failed to detect population expansion. (4) The long-term effective population size of humans is between 12,000 and 15,000. And (5) a non-African specific variant was found at a frequency of 35% in non-Africans, an estimate supported by the genotyping of additional 80 non-African and 106 African X chromosomes. This variant could have arisen in Eurasia more than 140,000 years ago, predating the emergence of modern humans. Moreover, this haplotype and all other haplotypes coalesced to the most recent common ancestor of the sample, which was estimated to be older than 490,000 years. Therefore, this region may have a long history in Eurasia.     

Life history determines genetic structure and evolutionary potential of host-parasite interactions

Measures of population genetic structure and diversity of disease-causing organisms are commonly used to draw inferences regarding their evolutionary history and potential to generate new variation in traits that determine interactions with their hosts. Parasite species exhibit a range of population structures and life-history strategies, including different transmission modes, life-cycle complexity, off-host survival mechanisms and dispersal ability. These are important determinants of the frequency and predictability of interactions with host species. Yet the complex causal relationships between spatial structure, life history and the evolutionary dynamics of parasite populations are not well understood. We demonstrate that a clear picture of the evolutionary potential of parasitic organisms and their demographic and evolutionary histories can only come from understanding the role of life history and spatial structure in influencing population dynamics and epidemiological patterns.     

Naturally rare versus newly rare: demographic inferences on two timescales inform conservation of Galápagos giant tortoises

Long‐term population history can influence the genetic effects of recent bottlenecks. Therefore, for threatened or endangered species, an understanding of the past is relevant when formulating conservation strategies. Levels of variation at neutral markers have been useful for estimating local effective population sizes (N_e) and inferring whether population sizes increased or decreased over time. Furthermore, analyses of genotypic, allelic frequency, and phylogenetic information can potentially be used to separate historical from recent demographic changes. For 15 populations of Galápagos giant tortoises (Chelonoidis sp.), we used 12 microsatellite loci and DNA sequences from the mitochondrial control region and a nuclear intron, to reconstruct demographic history on shallow (past ~100 generations, ~2500 years) and deep (pre‐Holocene, >10 thousand years ago) timescales. At the deep timescale, three populations showed strong signals of growth, but with different magnitudes and timing, indicating different underlying causes. Furthermore, estimated historical N_e of populations across the archipelago showed no correlation with island age or size, underscoring the complexity of predicting demographic history a priori. At the shallow timescale, all populations carried some signature of a genetic bottleneck, and for 12 populations, point estimates of contemporary N_e were very small (i.e., < 50). On the basis of the comparison of these genetic estimates with published census size data, N_e generally represented ~0.16 of the census size. However, the variance in this ratio across populations was considerable. Overall, our data suggest that idiosyncratic and geographically localized forces shaped the demographic history of tortoise populations. Furthermore, from a conservation perspective, the separation of demographic events occurring on shallow versus deep timescales permits the identification of naturally rare versus newly rare populations; this distinction should facilitate prioritization of management action.     

Spatial and temporal genetic dynamics of the grasshopper Oedaleus decorus revealed by museum genomics

Analyzing genetic variation through time and space is important to identify key evolutionary and ecological processes in populations. However, using contemporary genetic data to infer the dynamics of genetic diversity may be at risk of a bias, as inferences are performed from a set of extant populations, setting aside unavailable, rare, or now extinct lineages. Here, we took advantage of new developments in next‐generation sequencing to analyze the spatial and temporal genetic dynamics of the grasshopper Oedaleus decorus, a steppic Southwestern‐Palearctic species. We applied a recently developed hybridization capture (hyRAD) protocol that allows retrieving orthologous sequences even from degraded DNA characteristic of museum specimens. We identified single nucleotide polymorphisms in 68 historical and 51 modern samples in order to (i) unravel the spatial genetic structure across part of the species distribution and (ii) assess the loss of genetic diversity over the past century in Swiss populations. Our results revealed (i) the presence of three potential glacial refugia spread across the European continent and converging spatially in the Alpine area. In addition, and despite a limited population sample size, our results indicate (ii) a loss of allelic richness in contemporary Swiss populations compared to historical populations, whereas levels of expected heterozygosities were not significantly different. This observation is compatible with an increase in the bottleneck magnitude experienced by central European populations of O. decorus following human‐mediated land‐use change impacting steppic habitats. Our results confirm that application of hyRAD to museum samples produces valuable information to study genetic processes across time and space.     

Sometimes hidden but always there: the assumptions underlying genetic inference of demographic histories

Demographic processes directly affect patterns of genetic variation within contemporary populations as well as future generations, allowing for demographic inference from patterns of both present-day and past genetic variation. Advances in laboratory procedures, sequencing and genotyping technologies in the past decades have resulted in massive increases in high-quality genome-wide genetic data from present-day populations and allowed retrieval of genetic data from archaeological material, also known as ancient DNA. This has resulted in an explosion of work exploring past changes in population size, structure, continuity and movement. However, as genetic processes are highly stochastic, patterns of genetic variation only indirectly reflect demographic histories. As a result, past demographic processes need to be reconstructed using an inferential approach. This usually involves comparing observed patterns of variation with model expectations from theoretical population genetics. A large number of approaches have been developed based on different population genetic models that each come with assumptions about the data and underlying demography. In this article I review some of the key models and assumptions underlying the most commonly used approaches for past demographic inference and their consequences for our ability to link the inferred demographic processes to the archaeological and climate records.This article is part of the theme issue ‘Cross-disciplinary approaches to prehistoric demography’.     

Challenging views on the peopling history of East Asia: the story according to HLA markers

The peopling of East Asia by the first modern humans is strongly debated from a genetic point of view. A north-south genetic differentiation observed in this geographic area suggests different hypotheses on the origin of Northern East Asian (NEA) and Southern East Asian (SEA) populations. In this study, the highly polymorphic HLA markers were used to investigate East Asian genetic diversity. Our database covers a total of about 127,000 individuals belonging to 84 distinct Asian populations tested for HLA-A, -B, -C, -DPB1, and/or -DRB1 alleles. Many Chinese populations are represented, which have been sampled in the last 30 years but rarely taken into account in international research due to their data published in Chinese. By using different statistical methods, we found a significant correlation between genetics and geography and relevant genetic clines in East Asia. Additionally, HLA alleles appear to be unevenly distributed: some alleles observed in NEA populations are widespread at the global level, while some alleles observed in SEA populations are virtually unique in Asia. The HLA genetic variation in East Asia is also characterized by a decrease of diversity from north to south, although a reverse pattern appears when one only focuses on alleles restricted to Asia. These results reflect a more complex migration history than that illustrated by the "southern-origin" hypothesis, as genetic contribution of ancient human migrations through a northern route has probably been quite substantial. We thus suggest a new overlapping model where northward and southward opposite migrations occurring at different periods overlapped.     

Effective population size of natural populations of Drosophila buzzatii, with a comparative evaluation of nine methods of estimation

Allozyme and microsatellite data from numerous populations of Drosophila buzzatii have been used (i) to determine to what degree N(e) varies among generations within populations, and among populations, and (ii) to evaluate the congruence of four temporal and five single-sample estimators of N(e) . Effective size of different populations varied over two orders of magnitude, most populations are not temporally stable in genetic composition, and N(e) showed large variation over generations in some populations. Short-term N(e) estimates from the temporal methods were highly correlated, but the smallest estimates were the most precise for all four methods, and the most consistent across methods. Except for one population, N(e) estimates were lower when assuming gene flow than when assuming populations that were closed. However, attempts to jointly estimate N(e) and immigration rate were of little value because the source of migrants was unknown. Correlations among the estimates from the single-sample methods generally were not significant although, as for the temporal methods, estimates were most consistent when they were small. These single-sample estimates of current N(e) are generally smaller than the short-term temporal estimates. Nevertheless, population genetic variation is not being depleted, presumably because of past or ongoing migration. A clearer picture of current and short-term effective population sizes will only follow with better knowledge of migration rates between populations. Different methods are not necessarily estimating the same N(e) , they are subject to different bias, and the biology, demography and history of the population(s) may affect different estimators differently.     

Alleles versus mutations: Understanding the evolution of genetic architecture requires a molecular perspective on allelic origins

Perspectives on the role of large‐effect quantitative trait loci (QTL) in the evolution of complex traits have shifted back and forth over the past few decades. Different sets of studies have produced contradictory insights on the evolution of genetic architecture. I argue that much of the confusion results from a failure to distinguish mutational and allelic effects, a limitation of using the Fisherian model of adaptive evolution as the lens through which the evolution of adaptive variation is examined. A molecular‐based perspective reveals that allelic differences can involve the cumulative effects of many mutations plus intragenic recombination, a model that is supported by extensive empirical evidence. I discuss how different selection regimes could produce very different architectures of allelic effects under a molecular‐based model, which may explain conflicting insights on genetic architecture from studies of variation within populations versus between divergently selected populations. I address shortcomings of genome‐wide association study (GWAS) practices in light of more suitable models of allelic evolution, and suggest alternate GWAS strategies to generate more valid inferences about genetic architecture. Finally, I discuss how adopting more suitable models of allelic evolution could help redirect research on complex trait evolution toward addressing more meaningful questions in evolutionary biology.