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.     

Thirty‐five years of spatial autocorrelation analysis in population genetics: an essay in honour of Robert Sokal (1926–2012)

We could not start this review, literally from the beginning, without expressing our sadness over the passing of Professor Robert R. Sokal. We are sure, nevertheless, that the importance of his scientific achievements will ensure he is long remembered. In this modest tribute to Professor Sokal, we highlight his contributions to the field of population genetics and spatial statistical methods. Specifically, we discuss how two papers, co‐authored with Professor N. L. Oden and published in the pages of the Biological Journal of the Linnean Society in 1978, revolutionized the field of analytical population genetics. In these papers, Sokal and Oden created an elegant framework for inferring evolutionary processes (e.g. isolation‐by‐distance, demic diffusion, selection gradients, genetic drift) from the spatial autocorrelation analysis of genetic variation patterns. We also highlight the pivotal importance of Sokal's work to the development of emerging fields (e.g. landscape and conservation genetics). We hope this virtual issue containing the papers that Professor Sokal published in BJLS, and later, related papers by other researchers, will help to remember his work and maintain his legacy of spatial analysis in genetics, ecology, and evolutionary biology. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ??, ??–??.     

Estimating population structure from AFLP amplification intensity

In the last decade, amplified fragment length polymorphisms (AFLPs) have become one of the most widely used molecular markers to study the genetic structure of natural populations. Most of the statistical methods available to study the genetic structure of populations using AFLPs consider these markers as dominant and are thus unable to distinguish between individuals being heterozygous or homozygous for the dominant allele. Some attempts have been made to treat AFLPs as codominant markers by using AFLP band intensities to infer the most likely genotype of each individual. These two approaches have some drawbacks, the former discarding potentially valuable information and the latter being sometimes unable to correctly assign genotypes to individuals. In this study, we propose an alternative likelihood‐based approach, which does not attempt at inferring the genotype of each individual, but rather incorporate the uncertainty about genotypes into a Bayesian framework leading to the estimation of population‐specific F_IS and F_ST coefficients. We show with simulations that the accuracy of our method is much higher than one using AFLP as dominant markers and is generally close to what would be obtained by using the same number of Single‐Nucleotide Polymorphism (SNP) markers. The method is applied to a data set of four populations of the common vole (Microtus arvalis) from Grisons in Switzerland, for which we obtained 562 polymorphic AFLP markers. Our approach is very general and has the potential to make AFLP markers as useful as SNP data for nonmodel species.     

Fine‐scale genetic structure reflects sex‐specific dispersal strategies in a population of sociable weavers (Philetairus socius)

Dispersal is a critical driver of gene flow, with important consequences for population genetic structure, social interactions and other biological processes. Limited dispersal may result in kin‐structured populations in which kin selection may operate, but it may also increase the risk of kin competition and inbreeding. Here, we use a combination of long‐term field data and molecular genetics to examine dispersal patterns and their consequences for the population genetics of a highly social bird, the sociable weaver (Philetairus socius), which exhibits cooperation at various levels of sociality from nuclear family groups to its unique communal nests. Using 20 years of data, involving capture of 6508 birds and 3151 recaptures at 48 colonies, we found that both sexes exhibit philopatry and that any dispersal occurs over relatively short distances. Dispersal is female‐biased, with females dispersing earlier, further, and to less closely related destination colonies than males. Genotyping data from 30 colonies showed that this pattern of dispersal is reflected by fine‐scale genetic structure for both sexes, revealed by isolation by distance in terms of genetic relatedness and significant genetic variance among colonies. Both relationships were stronger among males than females. Crucially, significant relatedness extended beyond the level of the colony for both sexes. Such fine‐scale population genetic structure may have played an important role in the evolution of cooperative behaviour in this species, but it may also result in a significant inbreeding risk, against which female‐biased dispersal alone is unlikely to be an effective strategy.     

Spatial and population genetic structure of microsatellites in white pine

We evaluated the population genetic structure of seven microsatellite loci for old growth and second growth populations of eastern white pine (Pinus strobus). From each population, located within Hartwick Pines State Park, Grayling, Michigan, USA, 120-122 contiguous trees were sampled for genetic analysis. Within each population, genetic diversity was high and inbreeding low. When comparing these populations, there is a significant, but small (less than 1%), genetic divergence between populations. Spatial distance between populations or timber harvest at the second growth site were reasonable explanations for the observed minor differences in allele frequencies between populations. Spatial autocorrelation analysis suggested that, for the old growth population, weak positive structuring at 15 m fits the isolation by distance model for a neighbourhood size of about 100 individuals. In comparison, genotypes were randomly distributed in the second growth population. Thus, logging may have decreased spatial structuring at the second growth site, suggesting that management practices may be used to alter natural spatial patterns. In addition, the amount of autocorrelation in the old growth population appears to be lower for some of the microsatellites, suggesting higher numbers of rare alleles and that higher mutation rates may have directly affected spatial statistics by reducing structure.     

Genetic diversity,population structure and sex‐biased dispersal in three co‐evolving species

Genetic diversity and spatial structure of populations are important for antagonistic coevolution. We investigated genetic variation and population structure of three closely related European ant species: the social parasite Harpagoxenus sublaevis and its two host species Leptothorax acervorum and Leptothorax muscorum. We sampled populations in 12 countries and analysed eight microsatellite loci and an mtDNA sequence. We found high levels of genetic variation in all three species, only slightly less variation in the host L. muscorum. Using a newly introduced measure of differentiation (Jost’s D_est ), we detected strong population structuring in all species and less male‐biased dispersal than previously thought. We found no phylogeographic patterns that could give information on post‐glacial colonization routes – northern populations are as variable as more southern populations. We conclude that conditions for Thompson’s geographic mosaic of coevolution are ideal in this system: all three species show ample genetic variation and strong population structure.     

Sampling related individuals within ponds biases estimates of population structure in a pond‐breeding amphibian

Effective conservation and management of pond‐breeding amphibians depends on the accurate estimation of population structure, demographic parameters, and the influence of landscape features on breeding‐site connectivity. Population‐level studies of pond‐breeding amphibians typically sample larval life stages because they are easily captured and can be sampled nondestructively. These studies often identify high levels of relatedness between individuals from the same pond, which can be exacerbated by sampling the larval stage. Yet, the effect of these related individuals on population genetic studies using genomic data is not yet fully understood. Here, we assess the effect of within‐pond relatedness on population and landscape genetic analyses by focusing on the barred tiger salamanders (Ambystoma mavortium) from the Nebraska Sandhills. Utilizing genome‐wide SNPs generated using a double‐digest RADseq approach, we conducted standard population and landscape genetic analyses using datasets with and without siblings. We found that reduced sample sizes influenced parameter estimates more than the inclusion of siblings, but that within‐pond relatedness led to the inference of spurious population structure when analyses depended on allele frequencies. Our landscape genetic analyses also supported different models across datasets depending on the spatial resolution analyzed. We recommend that future studies not only test for relatedness among larval samples but also remove siblings before conducting population or landscape genetic analyses. We also recommend alternative sampling strategies to reduce sampling siblings before sequencing takes place. Biases introduced by unknowingly including siblings can have significant implications for population and landscape genetic analyses, and in turn, for species conservation strategies and outcomes.     

Genetic population structure in prickly sculpin (Cottus asper) reflects isolation‐by‐environment between two life‐history ecotypes

Life‐history transitions have evolved repeatedly in numerous taxa, although the ecological and evolutionary conditions favouring such transitions in the presence of gene flow remain poorly understood. The present study aimed to disentangle the effects of isolation‐by‐distance and isolation‐by‐environment on genetic differentiation between two sympatric life‐history ecotypes. Using 14 microsatellite loci, we first characterized amphidromous and freshwater groups of Cottus asper in a high gene flow setting in the Lower Fraser River system (south‐western British Columbia, Canada) to test for the effects of habitat and geographical distance on the distribution of life‐history ecotypes. Within the main river channel, no genetic differentiation was found, whereas tributaries even close to the estuary were genetically differentiated. Partial mantel tests confirmed that genetic differentiation between river tributaries and the main channel was independent from geographical distance, with distance‐scaled migration rates indicating reduced gene flow from the main channel into the tributaries. Our results suggest that isolation‐by‐environment can play an important role for the early stage of life‐history transitions, and may promote differentiation among life‐history ecotypes despite the presence of gene flow. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 943–957.     

Late Chachapoya population structure prior to Inka conquest

Archaeological and ethnohistorical documents suggest that the Chachapoya region was inhabited by a number of distinct sociopolitical groups that only united in the face of their common enemy, the Inka. The purpose of this research is to quantify the amount of internal genetic differentiation and levels of extraregional gene flow during the Late Chachapoya period, in order to obtain a better understanding of the genetic relationship between these presumed ethnic groups. Craniometric data were collected from three Late Chachapoya samples (Laguna Huayabamba, Kuelap, and Laguna de los Cóndores), in order to understand the genetic relationships between the groups and facilitate our understanding of Late Chachapoya population structure. Genetic differentiation among these series ranged from 0.047 (heritability = 1.0) to 0.090 (heritability = 0.55). The Relethford-Blangero residuals indicate that the Laguna Huayabamba and Laguna de los Cóndores populations were receiving greater than average external gene flow, while Kuelap was receiving less than average external gene flow. The correspondence between biological and archaeological data in the investigation of prehistoric ethnic identity is discussed.     

Population genetic structure of Arabidopsis lyrata in Europe

Population genetic theory predicts that the self-incompatible and perennial herb, Arabidopsis lyrata, will have a genetic structure that differs from the self-fertilizing, annual Arabidopsis thaliana. We quantified the genetic structure for eight populations of A. lyrata ssp. petraea in historically nonglaciated regions of central Europe. Analysis of 20 microsatellite loci for 344 individuals demonstrated that, in accordance with predictions, diploid populations had high genome-wide heterozygosity (H(O) = 0.48; H(E) = 0.52), high within-population diversity (83% of total) compatible with mutation-drift equilibrium, and moderate differentiation among populations (F(ST) = 0.17). Within a single population, the vast majority of genetic variability (92%) was found at the smallest spatial scale (< 3 m). Although there was no evidence of biparental inbreeding or clonal propagation at this scale (F(IS) = 0.003), significant fine-scale spatial autocorrelation indicated localized gene flow presumably due to gravity dispersed seeds (Sp = 0.018). Limited gene flow between isolated population clusters (regions) separated by hundreds of kilometres has given rise to an isolation by distance pattern of diversification, with low, but significant, differentiation among regions (F(ST) = 0.05). The maintenance of geographically widespread polymorphisms and uniformly high diversity throughout central Europe is consistent with periglacial survival of A. lyrata ssp. petraea north of the Alps in steppe-tundra habitats during the last glacial maximum. As expected of northern and previously glaciated localities, A. lyrata in Iceland was genetically less diverse and highly differentiated from central Europe (H(E) = 0.37; F(ST) = 0.27).     

Bayesian approaches for the analysis of population genetic structure: an example from Platanthera leucophaea (Orchidaceae)

We describe four extensions to existing Bayesian methods for the analysis of genetic structure in populations: (i) use of beta distributions to approximate the posterior distribution of f and theta(B); (ii) use of an entropy statistic to describe the amount of information about a parameter derived from the data; (iii) use of the Deviance Information Criterion (DIC) as a model choice criterion for determining whether there is evidence for inbreeding within populations or genetic differentiation among populations; and (iv) use of samples from the posterior distributions for f and theta(B) derived from different data sets to determine whether the estimates are consistent with one another. We illustrate each of these extensions by applying them to data derived from previous allozyme and random amplified polymorphic DNA surveys of an endangered orchid, Platanthera leucophaea, and we conclude that differences in theta(B) from the two data sets may represent differences in the underlying mutational processes.     

Moment estimation of population diversity and genetic distance from data on recessive markers

A moment-based method for estimating a measure of population diversity, theta or Wright's FST, is given for dominant markers such as amplified fragment length polymorphisms (AFLPs) or RAPDs in noninbred populations. Basic assumptions are that there is random mating, Hardy-Weinberg equilibrium, linkage equilibrium, no mutation from common ancestor and equally distant populations. It is based on the variances between and within populations of genotype frequencies, whereas previously moment methods for dominant markers have been indirect in that they have been based on first estimating allele frequencies and then using the variances of those frequencies. The use of genotype frequencies directly appears to be more robust. Approximate sampling errors of the estimates are given. Methods are extended to estimate genetic distances and their sampling errors. The AFLP data from samples of breeds of pig are used for illustration.     

Sex-specific genetic differentiation and coalescence times: estimating sex-biased dispersal rates

I derive the equilibrium values of sex-specific FST parameters, in an island model for a dioecious species with sex-biased dispersal and binomial distribution of family size before dispersal (as assumed in a Wright-Fisher population). I show that FST may take different values among males and among females whenever dispersal is a trait conditioned on gender. This has not always been recognized, because some models assumed that genes are sampled before dispersal. In particular, the ratios of sex-specific FST parameters evaluated after dispersal over FST evaluated before dispersal are simple functions of sex-specific dispersal rates. Therefore, a simple moment-based estimator of sex-specific dispersal rate is proposed. This method is based on the comparison of FST estimated before and after dispersal and assumes equilibrium between migration and drift. I evaluate this method through stochastic simulations for a range of sex-specific dispersal rates and sampling effort (sample size, number of loci scored).     

Exploring factors shaping population genetic structure of the freshwater fish Sinocyclocheilus grahami (Teleostei, Cyprinidae)

Phylogeographical analyses on Sinocyclocheilus grahami samples from seven localities within the Lake Dianchi Basin in China were conducted to explore the main factors shaping population structure within this species. Phylogenetic and network analyses revealed two major clades in 24 mtDNA haplotypes. One clade included three haplotypes exclusively from samples of the lower basin and another clade encompassed other haplotypes from samples of the upper basin. The estimated divergence time between the two clades predated the river capture event connecting the lower and upper lake basin and thus supported geographical isolation as the main factor shaping genetic divergence between these two clades. Furthermore, analysis of molecular variance and pair-wise Φ_ST distances revealed significant genetic differentiation within the upper basin. Mantel tests clearly supported patterns of differentiation arose purely as a result of isolation by distance. These results further highlight the importance of geographical isolation in shaping differentiation within this species.     

Evolution of population genetic structure of the British roe deer by natural and anthropogenic processes (Capreolus capreolus)

Human influence typically impacts on natural populations of conservation interest. These interactions are varied and sometimes complex, and may be negative and unintended or associated with conservation and management strategy. Understanding the details of how these interactions influence and are influenced by natural evolutionary processes is essential to the development of effective conservation strategies. In this study, we investigate a species in Britain that has experienced both negative impact through overhunting in historical times and management efforts through culls and translocations. At the same time, there are regional populations that have been less affected by human influence. We use mtDNA and nuclear microsatellite DNA markers to investigate patterns of connectivity and diversity and find multiple insular populations in Britain that probably evolved within the Holocene (when the habitat was free of ice). We identify three concurrent processes. First, surviving indigenous populations show highly provincial patterns of philopatry, maintaining and generating population structure on a small geographic scale. Second, founder populations into habitat extirpated of native populations have expanded, but remained largely insular. Third, introductions into established populations generate some admixture. We discuss the implications for the evolution of diversity of the integration of natural processes with anthropogenic influences on population size and distribution.     

Weak large‐scale population genetic structure in a philopatric seabird,the European Shag Phalacrocorax aristotelis

Quantifying population genetic structure is fundamental to testing hypotheses regarding gene flow, population divergence and dynamics across large spatial scales. In species with highly mobile life‐history stages, where it is unclear whether such movements translate into effective dispersal among discrete philopatric breeding populations, this approach can be particularly effective. We used seven nuclear microsatellite loci and mitochondrial DNA (ND2) markers to quantify population genetic structure and variation across 20 populations (447 individuals) of one such species, the European Shag, spanning a large geographical range. Despite high breeding philopatry, rare cross‐sea movements and recognized subspecies, population genetic structure was weak across both microsatellites and mitochondrial markers. Furthermore, although isolation‐by‐distance was detected, microsatellite variation provided no evidence that open sea formed a complete barrier to effective dispersal. These data suggest that occasional long‐distance, cross‐sea movements translate into gene flow across a large spatial scale. Historical factors may also have shaped contemporary genetic structure: cluster analyses of microsatellite data identified three groups, comprising colonies at southern, mid‐ and northern latitudes, and similar structure was observed at mitochondrial loci. Only one private mitochondrial haplotype was found among subspecies, suggesting that this current taxonomic subdivision may not be mirrored by genetic isolation.     

The socially parasitic ant Polyergus mexicanus has host‐associated genetic population structure and related neighbouring colonies

The genetic structure of populations can be both a cause and a consequence of ecological interactions. For parasites, genetic structure may be a consequence of preferences for host species or of mating behaviour. Conversely, genetic structure can influence where conspecific interactions among parasites lay on a spectrum from cooperation to conflict. We used microsatellite loci to characterize the genetic structure of a population of the socially parasitic dulotic (aka “slave‐making”) ant (Polyergus mexicanus), which is known for its host‐specificity and conspecific aggression. First, we assessed whether the pattern of host species use by the parasite has influenced parasite population structure. We found that host species use was correlated with subpopulation structure, but this correlation was imperfect: some subpopulations used one host species nearly exclusively, while others used several. Second, we examined the viscosity of the parasite population by measuring the relatedness of pairs of neighbouring parasitic ant colonies at varying distances from each other. Although natural history observations of local dispersal by queens suggested the potential for viscosity, there was no strong correlation between relatedness and distance between colonies. However, 35% of colonies had a closely related neighbouring colony, indicating that kinship could potentially affect the nature of some interactions between colonies of this social parasite. Our findings confirm that ecological forces like host species selection can shape the genetic structure of parasite populations, and that such genetic structure has the potential to influence parasite‐parasite interactions in social parasites via inclusive fitness.     

Range‐wide population genetic structure of the Caribbean sea fan coral,Gorgonia ventalina

The population structure of benthic marine organisms is of central relevance to the conservation and management of these often threatened species, as well as to the accurate understanding of their ecological and evolutionary dynamics. A growing body of evidence suggests that marine populations can be structured over short distances despite theoretically high dispersal potential. Yet the proposed mechanisms governing this structure vary, and existing empirical population genetic evidence is of insufficient taxonomic and geographic scope to allow for strong general inferences. Here, we describe the range‐wide population genetic structure of an ecologically important Caribbean octocoral, Gorgonia ventalina. Genetic differentiation was positively correlated with geographic distance and negatively correlated with oceanographically modelled dispersal probability throughout the range. Although we observed admixture across hundreds of kilometres, estimated dispersal was low, and populations were differentiated across distances <2 km. These results suggest that populations of G. ventalina may be evolutionarily coupled via gene flow but are largely demographically independent. Observed patterns of differentiation corroborate biogeographic breaks found in other taxa (e.g. an east/west divide near Puerto Rico), and also identify population divides not discussed in previous studies (e.g. the Yucatan Channel). High genotypic diversity and absence of clonemates indicate that sex is the primary reproductive mode for G. ventalina. A comparative analysis of the population structure of G. ventalina and its dinoflagellate symbiont, Symbiodinium, indicates that the dispersal of these symbiotic partners is not coupled, and symbiont transmission occurs horizontally.